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低功率光照疗法对机体免疫应答的影响
常好才1, 张真真2, 刘镭1     
1. 华南师范大学生物光子学研究院激光生命科学研究所,暨激光生命科学教育部重点实验室,广州 510631;
2. 中山大学中山医学院人类病毒研究所,广州 510080
摘要: 最近几年,采用红至红外波长(600~1 100 nm)的低功率光照(low-dose light,LDL)疗法对组织代谢系统、神经系统、血液循环系统和免疫系统等方面的调节效应已经引起了广泛关注.同时,生物能学和光生物学基础研究的发展推动了低功率光照在疾病治疗领域的革新.有报道指出,巨噬细胞、肥大细胞、中性粒细胞和淋巴细胞等免疫细胞能响应低功率光照,产生细胞因子和保护性的蛋白质分子来缓解一些疾病的进程.因此,本文将从分子、细胞和组织水平对低功率光照改善的一些疾病的免疫学现象及机制进行归纳总结.
关键词: 低功率光照     炎症反应     淋巴水肿     口咽黏膜炎     辐射性皮炎     抗肿瘤和抗菌    
Low-dose Light Therapy on Host Immune Response:Physiological Effects and Mechanisms of Action
CHANG Hao-Cai1, ZHANG Zhen-Zhen2, LIU Lei1     
1. MOE Key Laboratory of Laser Life Science & Institute of Laser Life Science, College of Biophotonics, South China Normal University, Guangzhou 510631, China;
2. Institute of Human Virology, Zhongshan School of Medicine, Sun Yat-sen University North Campus, Guangzhou 510080, China
*This work was supported by grants from The National Natural Science Foundation of China(61361160414, 31470072, 61405061) and the Natural Science Foundation of Guangdong Province, China (2014A030313419)
** Corresponding author: LIU Lei. Tel: 86-20-85211436, E-mail: liulei@scnu.edu.cn
Received: July 13, 2017 Accepted: October 19, 2017
Abstract: The effect of low-dose light (LDL) therapy, commonly using red and near infrared (NIR) light (600-1 100 nm), has gained attention in recent years as a relatively noninvasive technique in modulating the tissue metabolic system, nervous system, blood circulation system and immune system. The progress in the basic science fields of bioenergetics and photobiology has propelled LDL into the therapeutic revolution. The immune cells including macrophages, mast cells, neutrophils and lymphocytes as responder cells by LDL have been studied in the animals and humans with producing cytokines and protective proteins. The paper will review the mechanisms of immune action of LDL at the molecular, cellular, and tissue levels on mammalian.
Key words: Low-dose light     inflammatory reaction     lymphedema     oropharyngeal mucositis     radiation dermatitis     anti-infection and anti-tumor    

Since 1960s, Mester[1] discovered the biological effects of low-dose light (LDL) acting on biological tissue, LDL had gained attention by more and more researchers as a novel scientific approach, which induced nonthermal and nondestructive biological reactions, for therapeutic applications in a variety of experimental conditions. Patients, researchers and clinicians around the world are devoting attention to the potential therapeutic applications of LDL in immunity and other medical fields that have traditionally had a limited therapeutic contribution to patient care.

Recently, the use of LDL has extended beyond the realms of wound healing and pain, and recent research supports its potential applications in neurodegenerative diseases[2-3], type 2 diabetes[4], osteogenic differentiation[5] and thrombocytopenia[6-7]. However, the exact mechanisms of those effects induced by LDL are poorly understood, but the mechanism is probably to be photochemically related. Karu, a pioneer in the LDL field, proposed that cytochrome c oxidase (CcO) was the photoacceptor and signal transducer[8-9], which affected the mitochondrial electron transport system[10] and the biological regulation of reactive oxygen species (ROS)[11-14], adenosine triphosphate (ATP)[15], nitric oxide (NO)[16-17] and intracellular Ca2+[18-19], and further affected the ailment process including inflammation and cytokine and growth factor release (Figure 1). The article summarizes the available literature on molecular mechanisms of the protective or enhancing effects of LDL in a number of pathogenic conditions including inflammatory reaction, cancer therapyinduced complications (lymphedema, mucositis and dermatitis), and anti-infection and anti-tumor effects.

Fig. 1 The mechanism model of LDL Schematic diagram shows the red or near infrared (NIR) light is absorbed by the photoacceptors (e.g. cytochrome c oxidase) localized in mitochondria. During the process, ROS and ATP production are increased, NO is released, and intracellular Ca2+ concentration ([Ca2+]i) is elevated. These responses may ultimately lead to changes in cell morphology and function via activating some transcription factors[e.g., nuclear factor-κB (NF-κB), hypoxia inducible factor-1 (HIF-1), activator protein-1 (AP-1) and cAMP-response element binding protein (CREB)].
1 Reduced inflammatory reaction by LDL 1.1 LDL regulates the secretion of cytokines

Inflammatory reaction is the physiological reaction caused by the stimulation of trauma, bleeding or pathogen infection. It is the innate immune defensive reaction of immune cells and inflammatory factors. Over the years, several studies on humans and animals have shown that LDL has modulatory effects on inflammatory markers of IL-1β, IL-6, IL-8, TNF-α and prostaglandin E2 (PGE2), and relieves the inflammatory process (edema, necrosis, neutrophil cell influx, hemorrhagic formation). According to Chang et al.[20], inflammatory symptoms are caused by proinflammatory cytokines, such as IL-1β, IL-6 and TNF-α. Study by de Almeida and colleagues[21] reported LDL significantly decreased the inflammatory mediator levels of IL-1β, IL-6 and TNF-α in acute skeletal muscle injury. Similarly, LDL could reduced those cytokine production in the pathophysiology of osteoarthritis (OA)[22]. 25 J/cm2 LDL also decreased the level of pro-inflammatory cytokines of TNF-α, IL-1β, and IL-8 in rheumatoid arthritis synoviocytes[23]. Additionally, the trauma-induced pro-inflammatory state assessed by IL-6 and IL-10 was prevented LDL[24]. In parallel, LDL prevented trauma-induced reduction in BDNF and VEGF, vascular remodeling and fiber-proliferating markers. More recently, LDL has been shown very interesting effects on modulation of cyclooxygenase 2 (COX-2). (880± 10) nm LDL decreased the inflammatory cell influx and mRNA levels of COX-2 just in initial phase of Achilles tendinitis[25]. COX-2 mRNA expressions were also significantly decreased by treatment with 904 nm LDL[26]. Almeida et al[27]. also found that 904 nm LDL in 1.0 J group significantly decreases skeletal muscle damage through less COX-2-derived gene expression. However, the precise mechanism by which light affects the cytokines is not yet known. LDL probably modulated the pro-inflammatory cytokines by reducing the IL-1β and COX-2 mRNA expression and consequently reduced PGE2 levels by reducing cell migration and the quantity of macrophages, neutrophils, and mast cells in the injured tissue[28-29]. Macrophages and mast cells secrete the cytokine of IL-1β, which in turn recruits COX-2, an enzyme which converts arachidonic acid into PGE2[30-31]. From the above we see that reduced inflammatory reaction by LDL may depend not only on the light irradiation parameters (wave length, radiation dose), but also on pathological condition of the study model.

1.2 LDL increases MMPs and PA activity

Matrix metalloproteinases (MMPs), which are considered to degrade the components of the complex extracellular matrix, and plasminogen activator (PA), which is implicated in the plasminogen-plasmin proteolytic system, play a key role in extracellular matrix degradation, synthesis of kinin and fibrinolysis in the process of inflammation. Both 660 nm and 780 nm verified by Cury and colleagues could decrease MMP2 activity in a model of ischemic skin flap in rats[32]. And MMP9 activity was decreased on induced arthritis in the temporomandibular joint with 830 nm LDL treatment[33]. Additionally, several human and animal studies have shown that LDL with red to infrared wavelengths reduces the release of PA[34-35]. Thus, LDL probably modulates PA activity to degrade cell adhesive molecules and extracellular matrix proteins[36] through activation of MMPs[37]. Furthermore, plasminogen activates the kinin cascade via converting prekallikrein into kallikrein[38].

1.3 LDL modulates the immune cell activity

LDL also modulates the activity of mast cells, macrophages, neutrophils and lymphocytes to reduce the inflammatory process. Red LDL has been shown to induce the mast-cell degranulation[39-40], leading to the release of a multiple chemical mediators (VEGF121, VEGF165, VEGF189 and VEGF206) [41], which are related to vasodilation and vascular proliferation, and can optimize the inflammatory process[42]. Song et al.[43] reported that in rats LDL altered the macrophage polarization from M1 state to M2 state, which dampens the inflammatory and adaptive Th1 responses[44]. Other studies observed that LDL reduced in the absolute number of macrophages and neutrophils compared with the injury group[22, 45], resulting in decrease of secretion of pro-inflammatory cytokines and enzymes such as IL-6 and TNF-α involved in driving the inflammatory response[46]. For lymphocytes, LDL could activate directly its proliferation in vivo[47-49], leading to secrete anti-inflammatory cytokine of IL-10, which inhibited the production of pro-inflammatory cytokines and prevented macrophage and neutrophil infiltration into the injury[50]. Additionally, the presence of hemoglobin amplified the proliferation effect of LDL irradiation on lymphocyte culture[49]. Hemoglobin could catalyze free radical formation in the presence of hydrogen peroxide as in the Fenton reaction[51]. LDL at a given wavelength may promote ROS formation in a hemoglobin rich environment, and then the generation of an oxidative environment has a strong influence on T lymphocytes[52].

2 Reduced cancer therapy-induced complications by LDL

Not only drug resistance caused by chemotherapy and molecular targeted therapy is a major obstacle to the current tumor treatment[53-55], but also cancer therapy-induced complications are a common clinical problem. In human researches, LDL is widely studied to ameliorate cancer therapy-induced complications. Upper limb lymphedema, which is the result of the regional accumulation of amounts of protein-rich interstitial fluid caused by impaired lymph drainage[56], is a common complication of breast cancer surgery. To date, researchers have reported that LDL is benefit for postmastectomy lymphoedema[57-59] through presumably increasing microcirculation[60-61] to reduce the excessive amounts of tissue protein and fluid, and finally improve the limb performance. In particular, a study indicated that LDL was often within hours of irradiation as an efficacy treatment of lymphedema[62]. However, the molecular mechanisms of LDL in lymphoedema tissue remain elusive. At the microcirculatory level, the stimulatory/protective effects of LDL is achieved by modulating the angiogenic factor production by lymphocytes[63] and endothelial cells[64] in situ, then to accelerate spontaneous angiogenesis[65].

Oropharyngeal mucositis (OM), known as most painful oral lesions[66], is a major complication of head-and-neck oncologic therapy[67]. LDL was confirmed to be effective in controlling of OM caused by various cancer therapies[68-71]. Studies have unambiguously demonstrated that the mucositis pathogenesis are complex and associate with pro-inflammatory cytokines[72-73], microvascular injury[74], and extracellular matrix alterations[75-76]. Silva et al.[77] showed that LDL increased the levels of IL-10 in blood plasma and MMP-2 in saliva on 7th chemoradiotherapy-induced OM. Study by Oton-Leite[78] demonstrated that LDL significantly reduced salivary concentration of IL-6, EGF and VEGF during radiotherapy session. It seemingly suggested the mechanism of LDL-reduced the severity of OM caused by cancer therapy was linked to the modulation of proor anti-inflammatory cytokines, MMPs or growth factors. In an animal model of OM, studies have reported that LDL decreased the expression of COX-2[79], which elicits the synthesis of pro-inflammatory prostaglandins in malignant and inflamed tissues, and reduces the infiltration of neutrophils in inflamed tissues[80], thus further supporting the anti-inflammatory effect.

Radiation dermatitis (RD) occurs in a majority of breast cancer patients who receive radiotherapy and may exhibit symptoms such as redness, itching, dryness, and peeling skin[81]. DeLand et al.[82] showed that LDL reduced the incidence of skin reactions in breast cancer patients treated by radiotherapy postlumpectomy. Schindl and co-workers[83-84] demonstrated that LDL healed a long-lasting radiotherapy-induced skin ulcer. Regarding the mechanism of action, LDL have been demonstrated to induce neoangiogenesis via the activation of ERK/Sp1 pathway in vitro[64] and in vivo[83], to accelerate collateral circulation and enhance microcirculation[85], then to possibly improve skin circulation[86], and finally to reduce tissue damage caused by ischemia[87]. An alternative explanation of LDL-induced neoangiogenesis is via ROS[88], which lead to increase the level of HIF-1[89], then regulate the transcription of VEGF[90-91]. Additionally, LDL could modulate certain cellular proliferation and migration[92-94], and induce the secretion of fibroblast growth factor family involved in tissue repair[95]. Altogether, these findings suggested a beneficial effect of LDL on cancer therapy-induced complications and patients'quality of life in cancer patients.

3 Enhanced anti-infection and anti-tumor effect by LDL

Recently, the effect of LDL-induced antiinfection was further confirmed by Lu et al.[96]. They showed that LDL enhanced anti-infection ability in vivo to improve the macrophage phagocytic activity through Rac1-mediated signaling pathway. Simultaneously, Karunarathne et al.[97] showed that 488-, 515-, or 595-nm wavelength light could initiate macrophage migration. The production of pro-inflammatory cytokines (TNF-α and IL-1) by murine peritoneal macrophages in vitro and in vivo was raised by LDL accompanied with increasing the ability of bacterial killing[98]. In neutrophils, LDL also enhanced the ability to kill Candida albicans via the generation of ROS[99]. In a wound infection model, it was demonstrated LDL significantly decreased the incidences of microbial flora (Staphylococcus aureus and Bacillus subtilis) compared with placebo burns[100], and increased the amount of blood vessels, remodeled the collagen matrix, and matured collagen fibers in infected wounds[101].

The obvious parabola features of the biological effect of LDL on cells have been demonstrated by several studies[102-103]. With an increase of light output energy, its moderating action on cells can be increased gradually, but when the light output energy exceeds a certain threshold value, the inhibition effect of LDL emerges[104]. According to Lu and colleagues[105], high fluence, low-dose light (HF-LDL) was reported to kill tumor cell, leading to activate macrophages to create an immune memory response. A few molecular mechanisms revealed that HF-LDL-induced apoptotic tumor cells enhanced the pro-inflammatory cytokines (TNF-α and NO) production in macrophage, through upregulating NF-κB activity[106-107]. Those studies may provide an effective therapeutic approach to induce an antitumor immune response after HF-LDL treatment.

4 Conclusion

In conclusion, LDL has strong evidences for many beneficial effects on inflammatory reaction, cancer therapy-induced complications, and anti-infection and anti-tumor in animal models and human patients. In this review, LDL-induced those effects mainly involve 4 growth factors (FGF, EGF, TGF-β and VEGF), 5 interleukins (IL-1, IL-4, IL-6, IL-8 and IL-10), 5 inflammatory cytokines (PGE2, COX2, TNF-α, MMPs and PA) and 4 immune cells (macrophages, mast cells, neutrophils and lymphocytes). The mediator molecules induced/ upregulated by LDL are summarized(Table 1). However, the underlying mechanisms of those effects caused by LDL are not completely understood. The precise molecular mechanisms are still needed to further experiments for propelling LDL into the therapeutic revolution.

Table 1 Mediator molecules associated with LDL
References
[1] Mester E, Mester A F, Mester A. The biomedical effects of laser application on biological systems. Laser Rev, 1968, 1: 3
[2] Gu X, Liu L, Shen Q, et al. Photoactivation of ERK/CREB/VMAT2 pathway attenuates MPP+-induced neuronal injury in a cellular model of Parkinson's disease. Cellular Signalling, 2017, 37: 103-114 DOI:10.1016/j.cellsig.2017.06.007
[3] Meng C B, He Z Y, Xing D. Low-level laser therapy rescues dendrite atrophy via upregulating BDNF expression: implications for Alzheimer's disease. Journal of Neuroscience, 2013, 33(33): 13505-13517 DOI:10.1523/JNEUROSCI.0918-13.2013
[4] Jiang X, Huang L, Xing D. Photoactivation of Dok1/ERK/ PPARgamma signaling axis inhibits excessive lipolysis in insulin-resistant adipocytes. Cellular Signalling, 2015, 27(7): 1265-1275 DOI:10.1016/j.cellsig.2015.03.010
[5] Feng J, Sun Q, Liu L, et al. Photoactivation of TAZ via Akt/GSK3beta signaling pathway promotes osteogenic differentiation. The international Journal of Biochemistry & Cell Biology, 2015, 66: 59-68
[6] Zhang Q, Dong T T, Li P Y, et al. Noninvasive low-level laser therapy for thrombocytopenia. Sci Transl Med, 2016, 8(349): 349ra101 DOI:10.1126/scitranslmed.aaf4964
[7] Yang J K, Zhang Q, Li P Y, et al. Low-level light treatment ameliorates immune thrombocytopenia. Scientific Reports, 2016, 6: srep38238 DOI:10.1038/srep38238
[8] Karu T I. Mitochondrial signaling in mammalian cells activated by red and near-IR radiation. Photochemistry and Photobiology, 2008, 84(5): 1091-1099
[9] Karu T I, Pyatibrat L V, Moskvin S V, et al. Elementary processes in cells after light absorption do not depend on the degree of polarization: Implications for the mechanisms of laser phototherapy. Photomedicine and Laser Surgery, 2008, 26(2): 77-82 DOI:10.1089/pho.2007.2134
[10] Yu W, Naim J O, Mcgowan M, et al. Photomodulation of oxidative metabolism and electron chain enzymes in rat liver mitochondria. Photochemistry and Photobiology, 1997, 66(6): 866-871
[11] Zhang J T, Xing D, Gao X J. Low-power laser irradiation activates Src tyrosine kinase through reactive oxygen species-mediated signaling pathway. Journal of Cellular Physiology, 2008, 217(2): 518-528
[12] Sun X G, Wu S N, Xing D. The reactive oxygen species-Src-Stat3 pathway provokes negative feedback inhibition of apoptosis induced by high-fluence low-power laser irradiation. Febs Journal, 2010, 277(22): 4789-4802 DOI:10.1111/j.1742-4658.2010.07884.x
[13] Chen P J, Luo X Y, Nie P P, et al. CQ synergistically sensitizes human colorectal cancer cells to SN-38/CPT-11 through lysosomal and mitochondrial apoptotic pathway via p53-ROS cross-talk. Free Radical Bio Med, 2017, 104: 280-297 DOI:10.1016/j.freeradbiomed.2017.01.033
[14] Arany P R, Cho A, Hunt T D, et al. Photoactivation of endogenous latent transforming growth factor-beta 1 directs dental stem cell differentiation for regeneration. Sci Transl Med, 2014, 6(238): 238ra69 DOI:10.1126/scitranslmed.3008234
[15] Blatt A, Elbaz-Greener G A, Tuby H, et al. Low-level laser therapy to the bone marrow reduces scarring and improves heart function post-acute myocardial infarction in the pig. Photomedicine and Laser Surgery, 2016, 34(11): 516-524 DOI:10.1089/pho.2015.3988
[16] Guerra F D, Vieira C P, Oliveira L P, et al. Low-level laser therapy modulates pro-inflammatory cytokines after partial tenotomy. Lasers in Medical Science, 2016, 31(4): 759-766 DOI:10.1007/s10103-016-1918-7
[17] Farivar S, Malekshahabi T, Shiari R. Biological effects of low level laser therapy. Journal of lasers in Medical Sciences, 2014, 5(2): 58-62
[18] Mang T S, Maneshi M M, Shucard D W, et al. Effects of low-level laser exposure on calcium channels and intracellular release in cultured astrocytes. Lasers in Surgery & Medicine, 2015, 47(4): 383
[19] De Freitas L F, Hamblin M R. Proposed mechanisms of photobiomodulation or low-level light therapy. Ieee J Sel Top Quant, 2016, 22(3): pii7000417
[20] Chang X Y, He H, Zhu L P, et al. Protective effect of apigenin on Freund's complete adjuvant-induced arthritis in rats via inhibiting P2X7/NF-kappa B pathway. Chemico-Biological Interactions, 2015, 236: 41-46 DOI:10.1016/j.cbi.2015.04.021
[21] De Almeida P, Tomazoni S S, Frigo L, et al. What is the best treatment to decrease pro-inflammatory cytokine release in acute skeletal muscle injury induced by trauma in rats: low-level laser therapy, diclofenac, or cryotherapy?. Lasers in Medical Science, 2014, 29(2): 653-658 DOI:10.1007/s10103-013-1377-3
[22] Alves A C A, Vieira R D, Leal E C P, et al. Effect of low-level laser therapy on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Arthritis Res Ther, 2013, 15(5): R116 DOI:10.1186/ar4296
[23] Yamaura M, Yao M, Yaroslavsky I, et al. Low level light effects on inflammatory cytokine production by rheumatoid arthritis synoviocytes. Lasers in Surgery and Medicine, 2009, 41(4): 282-290
[24] Silveira P C L, Scheffer D D, Glaser V, et al. Low-level laser therapy attenuates the acute inflammatory response induced by muscle traumatic injury. Free Radical Res, 2016, 50(5): 503-513 DOI:10.3109/10715762.2016.1147649
[25] Xavier M, David D R, De Souza R A, et al. Anti-inflammatory effects of low-level light emitting diode therapy on achilles tendinitis in rats. Lasers in Surgery and Medicine, 2010, 42(6): 553-558
[26] Leal E C P, De Almeida P, Tomazoni S S, et al. Superpulsed low-level laser therapy protects skeletal muscle of mdx mice against damage, inflammation and morphological changes delaying dystrophy progression. PloS One, 2014, 9(3): e89453 DOI:10.1371/journal.pone.0089453
[27] De Almeida P, Lopes-Martins R a B, Tomazoni S S, et al. Lowlevel laser therapy improves skeletal muscle performance, decreases skeletal muscle damage and modulates mRNA expression of COX-1 and COX-2 in a dose-dependent manner. Photochemistry and Photobiology, 2011, 87(5): 1159-1163
[28] Dourado D M, Favero S, Matias R, et al. Low-level laser therapy promotes vascular endothelial growth factor receptor-1 expression in endothelial and nonendothelial cells of mice gastrocnemius exposed to snake venom. Photochemistry and Photobiology, 2011, 87(2): 418-426
[29] Silveira L B, Prates R A, Novelli M D, et al. Investigation of mast cells in human gingiva following low-intensity laser irradiation. Photomedicine and Laser Surgery, 2008, 26(4): 315-321 DOI:10.1089/pho.2007.2140
[30] Hardy M M, Seibert K, Manning P T, et al. Cyclooxygenase 2-dependent prostaglandin E-2 modulates cartilage proteoglycan degradation in human osteoarthritis explants. Arthritis and Rheumatism, 2002, 46(7): 1789-1803
[31] Marsolais D, Cote C H, Frenette K. Neutrophils and macrophages accumulate sequentially following Achilles tendon injury. J Orthopaed Res, 2001, 19(6): 1203-1209 DOI:10.1016/S0736-0266(01)00031-6
[32] Cury V, Moretti A I S, Assis L, et al. Low level laser therapy increases angiogenesis in a model of ischemic skin flap in rats mediated by VEGF, HIF-1 alpha and MMP-2. J Photoch Photobio B, 2013, 125: 164-170 DOI:10.1016/j.jphotobiol.2013.06.004
[33] Lemos G A, Rissi R, Pires I L D, et al. Low-level laser therapy stimulates tissue repair and reduces the extracellular matrix degradation in rats with induced arthritis in the temporomandibular joint. Lasers in Medical Science, 2016, 31(6): 1051-1059 DOI:10.1007/s10103-016-1946-3
[34] Vanin A A, De Marchi T, Tomazoni S S, et al. Pre-exercise infrared low-level laser therapy (810 nm) in skeletal muscle performance and postexercise recovery in humans, what is the optimal dose? A randomized, double-blind, placebo-controlled clinical trial. Photomedicine and Laser Surgery, 2016, 34(10): 473-482 DOI:10.1089/pho.2015.3992
[35] Takema T, Yamaguchi M, Abiko Y. Reduction of plasminogen activator activity stimulated by lipopolysaccharide from periodontal pathogen in human gingival fibroblasts by low-energy laser irradiation. Lasers in Medical Science, 2000, 15(1): 35-42 DOI:10.1007/s101030050045
[36] Castellino F J. Biochemistry of human plasminogen. Seminars in Thrombosis and Hemostasis, 1984, 10(1): 18-23 DOI:10.1055/s-2007-1004404
[37] Werb Z, Mainardi C L, Vater C A, et al. Endogenous activation of latent collagenase by rheumatoid synovial cells. Evidence for a role of plasminogen activator. The New England Journal of Medicine, 1977, 296(18): 1017-1023 DOI:10.1056/NEJM197705052961801
[38] Vogt W. Kinin formation by plasmin, an indirect process mediated by activation of kallikrein. The Journal of Physiology, 1964, 170: 153-166 DOI:10.1113/jphysiol.1964.sp007320
[39] Wang L, Zhang D, Schwarz W. TRPV channels in mast cells as a target for low-level-laser therapy. Cells, 2014, 3(3): 662-673 DOI:10.3390/cells3030662
[40] Yang W Z, Chen J Y, Yu J T, et al. Effects of low power laser irradiation on intracellular calcium and histamine release in RBL2H3 mast cells. Photochemistry and Photobiology, 2007, 83(4): 979-984 DOI:10.1111/j.1751-1097.2007.00116.x
[41] Pereira M C M C, De Pinho C B, Medrado A R P, et al. Influence of 670 nm low-level laser therapy on mast cells and vascular response of cutaneous injuries. J Photoch Photobio B, 2010, 98(3): 188-192 DOI:10.1016/j.jphotobiol.2009.12.005
[42] Paraguassu G M, De Castro I C V, Vasconcelosa R M, et al. Effect of LED phototherapy (lambda 630 +/-20 nm) on mast cells during wound healing in hypothyroid. Proc SPIE, 2014, 8932: 893216-893216 DOI:10.1117/12.2039880
[43] Song J W, Li K, Liang Z W, et al. Low-level laser facilitates alternatively activated macrophage/microglia polarization and promotes functional recovery after crush spinal cord injury in rats. Scientific Reports, 2017, 7(1): 620 DOI:10.1038/s41598-017-00553-6
[44] Bouhlel M A, Derudas B, Rigamonti E, et al. PPAR gamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metabolism, 2007, 6(2): 137-143 DOI:10.1016/j.cmet.2007.06.010
[45] Dos Santos S A, Alves A C, Leal-Junior E C, et al. Comparative analysis of two low-level laser doses on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Lasers in Medical Science, 2014, 29(3): 1051-1058
[46] Kennedy A, Fearon U, Veale D J, et al. Macrophages in synovial inflammation. Frontiers in Immunology, 2011, 2: 52
[47] Avci P, Gupta A, Sadasivam M, et al. Low-level laser (light) therapy (LLLT) in skin: stimulating, healing, restoring. Semin Cutan Med Surg, 2013, 32(1): 41-52
[48] Manteifel V, Bakeeva L, Karu T. Ultrastructural changes in chondriome of human lymphocytes after irradiation with He-Ne laser: Appearance of giant mitochondria. J Photoch Photobio B, 1997, 38(1): 25-30 DOI:10.1016/S1011-1344(96)07426-X
[49] Stadler I, Evans R, Kolb B, et al. In vitro effects of low-level laser irradiation at 660 nm on peripheral blood lymphocytes. Lasers in Surgery and Medicine, 2000, 27(3): 255-261
[50] Efron P A, Moldawer L L. Cytokines and wound healing: the role of cytokine and anticytokine therapy in the repair response. The Journal of Burn care & Rehabilitation, 2004, 25(2): 149-160
[51] Gutteridge J M. Iron promoters of the Fenton reaction and lipid peroxidation can be released from haemoglobin by peroxides. FEBS Letters, 1986, 201(2): 291-295 DOI:10.1016/0014-5793(86)80626-3
[52] Cemerski S, Cantagrel A, Van Meerwijk J P, et al. Reactive oxygen species differentially affect T cell receptor-signaling pathways. The Journal of Biological Chemistry, 2002, 277(22): 19585-19593 DOI:10.1074/jbc.M111451200
[53] Zhu J, Zou Z Z, Nie P P, et al. Downregulation of microRNA27b-3p enhances tamoxifen resistance in breast cancer by increasing NR5A2 and CREB1 expression. Cell Death Dis, 2016, 7(11): e2454 DOI:10.1038/cddis.2016.361
[54] Ao X, Nie P P, Wu B Y, et al. Decreased expression of microRNA17 and microRNA-20b promotes breast cancer resistance to taxol therapy by upregulation of NCOA3. Cell Death Dis, 2016, 7(11): e2463 DOI:10.1038/cddis.2016.367
[55] Zou Z Z, Yuan Z Y, Zhang Q X, et al. Aurora kinase A inhibitioninduced autophagy triggers drug resistance in breast cancer cells. Autophagy, 2012, 8(12): 1798-1810 DOI:10.4161/auto.22110
[56] Rockson S G. Lymphedema. American Journal Of Medicine, 2001, 110(4): 288-295 DOI:10.1016/S0002-9343(00)00727-0
[57] Smoot B, Chiavola-Larson L, Lee J, et al. Effect of low-level laser therapy on pain and swelling in women with breast cancer-related lymphedema: a systematic review and meta-analysis. J Cancer Surviv, 2015, 9(2): 287-304 DOI:10.1007/s11764-014-0411-1
[58] Ridner S H, Poage-Hooper E, Kanar C, et al. A pilot randomized trial evaluating low-level laser therapy as an alternative treatment to manual lymphatic drainage for breast cancer-related lymphedema. Oncol Nurs Forum, 2013, 40(4): 383-393 DOI:10.1188/13.ONF.383-393
[59] Hwang W T, Chung S H, Lee J S. Complex decongestive physical therapy and low-level laser therapy for the treatment of pediatric congenital lymphedema: a case report. J Phys Ther Sci, 2015, 27(6): 2021-2022 DOI:10.1589/jpts.27.2021
[60] Kozanoglu E, Basaran S, Paydas S, et al. Efficacy of pneumatic compression and low-level laser therapy in the treatment of postmastectomy lymphoedema: a randomized controlled trial. Clinical Rehabilitation, 2009, 23(2): 117-124 DOI:10.1177/0269215508096173
[61] Oremus M, Dayes I, Walker K, et al. Systematic review: conservative treatments for secondary lymphedema. BMC Cancer, 2012, 12: 6 DOI:10.1186/1471-2407-12-6
[62] Carati C J, Anderson S N, Gannon B J, et al. Treatment of postmastectomy lymphedema with low-level laser therapy: a double blind, placebo-controlled trial. Cancer, 2003, 98(6): 1114-1122
[63] Agaiby A D, Ghali L R, Wilson R, et al. Laser modulation of angiogenic factor production by T-lymphocytes. Lasers in Surgery and Medicine, 2000, 26(4): 357-363
[64] Feng J, Zhang Y J, Xing D. Low-power laser irradiation (LPLI) promotes VEGF expression and vascular endothelial cell proliferation through the activation of ERK/Sp1 pathway. Cellular Signalling, 2012, 24(6): 1116-1125 DOI:10.1016/j.cellsig.2012.01.013
[65] Park I S, Chung P S, Ahn J C. Adipose-derived stem cell spheroid treated with low-level light irradiation accelerates spontaneous angiogenesis in mouse model of hindlimb ischemia. Cytotherapy, 2017, 19(9): 1070-1078 DOI:10.1016/j.jcyt.2017.06.005
[66] Cauwels R G, Martens L C. Low level laser therapy in oral mucositis: a pilot study. European Archives of Paediatric Dentistry: Official Journal of the European Academy of Paediatric Dentistry, 2011, 12(2): 118-123 DOI:10.1007/BF03262791
[67] Gouvea De Lima A, Villar R C, De Castro G, Jr, et al. Oral mucositis prevention by low-level laser therapy in head-and-neck cancer patients undergoing concurrent chemoradiotherapy: a phase Ⅲ randomized study. International Journal of Radiation Oncology, Biology, Physics, 2012, 82(1): 270-275 DOI:10.1016/j.ijrobp.2010.10.012
[68] Arbabi-Kalati F, Arbabi-Kalati F, Moridi T. Evaluation of the effect of low level laser on prevention of chemotherapy-induced mucositis. Acta Medica Iranica, 2013, 51(3): 157-162
[69] Gautam A P, Fernandes D J, Vidyasagar M S, et al. Low level laser therapy against radiation induced oral mucositis in elderly head and neck cancer patients-a randomized placebo controlled trial. Journal of Photochemistry and Photobiology B, Biology, 2015, 144: 51-56 DOI:10.1016/j.jphotobiol.2015.01.011
[70] Oberoi S, Zamperlini-Netto G, Beyene J, et al. Effect of prophylactic low level laser therapy on oral mucositis: a systematic review and meta-analysis. PloS One, 2014, 9(9): e107418 DOI:10.1371/journal.pone.0107418
[71] Allan E, Barney C, Baum S, et al. Low-level laser therapy and laser debridement for management of oral mucositis in patients with head and neck cancer receiving chemotherapy and radiation. Int J Radiat Oncol, 2016, 94(4): 883
[72] Ong Z Y, Gibson R J, Bowen J M, et al. Pro-inflammatory cytokines play a key role in the development of radiotherapyinduced gastrointestinal mucositis. Radiation Oncology, 2010, 5: 22 DOI:10.1186/1748-717X-5-22
[73] Logan R, Stringer A, Bowen J, et al. Is the pathobiology of chemotherapy-induced alimentary tract mucositis influenced by the type of mucotoxic drug administered?. Cancer Chemoth Pharm, 2009, 63(2): 239-251 DOI:10.1007/s00280-008-0732-8
[74] Hamilton S, Yoo J, Hammond A, et al. Microvascular changes in radiation-induced oral mucositis. Journal of Otolaryngology-Head & Neck Surgery= Le Journal d'oto-rhino-laryngologie et de chirurgie cervico-faciale, 2008, 37(5): 730-737
[75] Al-Dasooqi N, Bowen J M, Gibson R J, et al. Irinotecan-induced alterations in intestinal cell kinetics and extracellular matrix component expression in the Dark Agouti rat. International Journal of Experimental Pathology, 2011, 92(5): 357-365 DOI:10.1111/iep.2011.92.issue-5
[76] Sonis S T. The pathobiology of mucositis. Nature Reviews Cancer, 2004, 4(4): 277-284 DOI:10.1038/nrc1318
[77] Silva G B L, Sacono N T, Othon-Leite A F, et al. Effect of low-level laser therapy on inflammatory mediator release during chemotherapy-induced oral mucositis: a randomized preliminary study. Lasers in Medical Science, 2015, 30(1): 117-126 DOI:10.1007/s10103-014-1624-2
[78] Oton-Leite A F, Silva G B L, Morais M O, et al. Effect of low-level laser therapy on chemoradiotherapy-induced oral mucositis and salivary inflammatory mediators in head and neck cancer patients. Lasers in Surgery and Medicine, 2015, 47(4): 296-305
[79] Lopes N N F, Plapler H, Chavantes M C, et al. Cyclooxygenase-2 and vascular endothelial growth factor expression in 5-fluorouracil-induced oral mucositis in hamsters: evaluation of two low-intensity laser protocols. Supportive Care In Cancer, 2009, 17(11): 1409-1415 DOI:10.1007/s00520-009-0603-9
[80] Lopes N N F, Plapler H, Lalla R V, et al. Effects of low-level laser therapy on collagen expression and neutrophil infiltrate in 5-fluorouracil-induced oral mucositis in hamsters. Lasers in Surgery and Medicine, 2010, 42(6): 546-552
[81] Censabella S, Claes S, Robijns J, et al. Photobiomodulation for the management of radiation dermatitis: the DERMIS trial, a pilot study of MLS (R) laser therapy in breast cancer patients. Supportive Care In Cancer, 2016, 24(9): 3925-3933 DOI:10.1007/s00520-016-3232-0
[82] Deland M M, Weiss R A, Mcdaniel D H, et al. Treatment of radiation-induced dermatitis with light-emitting diode (LED) photomodulation. Lasers in Surgery and Medicine, 2007, 39(2): 164-168
[83] Schindl A, Schindl M, Schindl L, et al. Increased dermal angiogenesis after low-intensity laser therapy for a chronic radiation ulcer determined by a video measuring system. J Am Acad Dermatol, 1999, 40(3): 481-484 DOI:10.1016/S0190-9622(99)70503-7
[84] Schindl M, Kerschan K, Schindl A, et al. Induction of complete wound healing in recalcitrant ulcers by low-intensity laser irradiation depends on ulcer cause and size. Photodermatol Photo, 1999, 15(1): 18-21
[85] Ihsan F R M. Low-level laser therapy accelerates collateral circulation and enhances microcirculation. Photomedicine and Laser Surgery, 2005, 23(3): 289-294 DOI:10.1089/pho.2005.23.289
[86] Chawla K, Lamba A K, Tandon S, et al. Effect of low-level laser therapy on wound healing after depigmentation procedure: A clinical study. Journal of Indian Society of Periodontology, 2016, 20(2): 184-188
[87] de Lima F M, Albertini R, Dantas Y, et al. Low-level laser therapy restores the oxidative stress balance in acute lung injury induced by gut ischemia and reperfusion. Photochem Photobiol, 2013, 89(1): 179-188 DOI:10.1111/j.1751-1097.2012.01214.x
[88] Ushio-Fukai M, Alexander R W. Reactive oxygen species as mediators of angiogenesis signaling -Role of NAD(P)H oxidase. Molecular and Cellular Biochemistry, 2004, 264(1-2): 85-97
[89] Irwin D C, Mccord J M, Nozik-Grayck E, et al. A potential role for reactive oxygen species and the HIF-1 alpha-VEGF pathway in hypoxia-induced pulmonary vascular leak. Free Radical Bio Med, 2009, 47(1): 55-61 DOI:10.1016/j.freeradbiomed.2009.03.027
[90] He Y, Fan J, Lin H, et al. The anti-malaria agent artesunate inhibits expression of vascular endothelial growth factor and hypoxiainducible factor-1alpha in human rheumatoid arthritis fibroblastlike synoviocyte. Rheumatology International, 2011, 31(1): 53-60 DOI:10.1007/s00296-009-1218-7
[91] Molitoris K H, Kazi A A, Koos R D. Inhibition of oxygen-induced hypoxia-inducible factor-1alpha degradation unmasks estradiol induction of vascular endothelial growth factor expression in ECC-1 cancer cells in vitro. Endocrinology, 2009, 150(12): 5405-5414 DOI:10.1210/en.2009-0884
[92] Gao X J, Chen T S, Xing D, et al. Single cell analysis of PKC activation during proliferation and apoptosis induced by laser irradiation. Journal of Cellular Physiology, 2006, 206(2): 441-448
[93] Huang L, Jiang X X, Gong L L, et al. Photoactivation of Akt1/GSK3 isoform-specific signaling axis promotes pancreaticcell regeneration. Journal of Cellular Biochemistry, 2015, 116(8): 1741-1754 DOI:10.1002/jcb.v116.8
[94] Basso F G, Soares D G, Pansani T N, et al. Proliferation, migration, and expression of oral-mucosal-healing-related genes by oral fibroblasts receiving low-level laser therapy after inflammatory cytokines challenge. Lasers in Surgery and Medicine, 2016, 48(10): 1006-1014
[95] Bensadoun R J, Nair R G. Low-level laser therapy in the management of mucositis and dermatitis induced by cancer therapy. Photomedicine and Laser Surgery, 2015, 33(10): 487-491 DOI:10.1089/pho.2015.4022
[96] Lu C X, Fan Z J, Xing D. Photo-enhancement of macrophage phagocytic activity via Rac1-mediated signaling pathway: Implications for bacterial infection. Int J Biochem Cell B, 2016, 78: 206-216 DOI:10.1016/j.biocel.2016.06.010
[97] Karunarathne W K A, Giri L, Patel A K, et al. Optical control demonstrates switch-like PIP3 dynamics underlying the initiation of immune cell migration. Proc Natl Acad Sci USA, 2013, 110(17): E1575-E1583 DOI:10.1073/pnas.1220755110
[98] Rudik D V, Tikhomirova E I. Activity of murine peritoneal macrophages upon weak red and infrared laser irradiation in vitro and in vivo. Biophysics, 2007, 52(5): 504-507 DOI:10.1134/S0006350907050090
[99] Cerdeira C D, Brigagao M R P L, De Carli M L, et al. Low-level laser therapy stimulates the oxidative burst in human neutrophils and increases their fungicidal capacity. Journal of Biophotonics, 2016, 9(11-12): 1180-1188 DOI:10.1002/jbio.201600035
[100] Ezzati A, Bayat M, Khoshvaghti A. Low-level laser therapy with a pulsed infrared laser accelerates second-degree burn healing in rat: a clinical and microbiologic study. Photomedicine and Laser Surgery, 2010, 28(5): 603-611 DOI:10.1089/pho.2009.2544
[101] Santos N R S, Sobrinho J B D, Almeida P F, et al. Influence of the combination of infrared and red laser light on the healing of cutaneous wounds infected by staphylococcus aureus. Photomedicine and Laser Surgery, 2011, 29(3): 177-182 DOI:10.1089/pho.2009.2749
[102] Hawkins D, Abrahamse H. Effect of multiple exposures of low-level laser therapy on the cellular responses of wounded human skin fibroblasts. Photomedicine and Laser Surgery, 2006, 24(6): 705-714 DOI:10.1089/pho.2006.24.705
[103] Frigo L, Favero G M, Lima H J C, et al. Low-level laser irradiation (InGaAlP-660 nm) increases fibroblast cell proliferation and reduces cell death in a dose-dependent manner. Photomedicine and Laser Surgery, 2010, 28(S1): S151-S156
[104] Wu S N, Xing D. Intracellular signaling cascades following light irradiation. Laser Photonics Rev, 2014, 8(1): 115-130 DOI:10.1002/lpor.201300015
[105] Lu C X, Zhou F F, Wu S N, et al. Phototherapy-induced antitumor immunity: long-term tumor suppression effects via photoinactivation of respiratory chain oxidase-triggered superoxide anion burst. Antioxid Redox Sign, 2016, 24(5): 249-262 DOI:10.1089/ars.2015.6334
[106] Wei Y, Xing D. Phototherapy-treated apoptotic tumor cells induce pro-inflammatory cytokines production in macrophage. Twelfth International Conference on Photonics and Imaging in Biology and Medicine, 2014, 7160(2): 71601S-71601S
[107] Zhou F, Xing D. HF-LPLI-treated tumor cells induce NO production in macrophage. Proc SPIE, 2013, 8582(16): 7629-7638
[108] Sonis S T, Hashemi S, Epstein J B, et al. Could the biological robustness of low level laser therapy (Photobiomodulation) impact its use in the management of mucositis in head and neck cancer patients. Oral Oncology, 2016, 54: 7-14 DOI:10.1016/j.oraloncology.2016.01.005
中国科学院生物物理研究所和中国生物物理学会共同主办
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文章信息

常好才, 张真真, 刘镭
CHANG Hao-Cai, ZHANG Zhen-Zhen, LIU Lei
低功率光照疗法对机体免疫应答的影响
Low-dose Light Therapy on Host Immune Response:Physiological Effects and Mechanisms of Action
生物化学与生物物理进展, 2017, 44(12): 1074-1082
Progress in Biochemistry and Biophysics, 2017, 44(12): 1074-1082
http://dx.doi.org/10.16476/j.pibb.2017.0275

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收稿日期: 2017-07-13
接受日期: 2017-10-19

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