Mitochondrial quality control in intervertebral disc degeneration

다국어 초록 (Multilingual Abstract)

Intervertebral disc degeneration (IDD) is a common and early-onset pathogenesis in the human lifespan that can increase the risk of low back pain. More clarification of the molecular mechanisms associated with the onset and progression of IDD is likely to help establish novel preventive and therapeutic strategies. Recently, mitochondria have been increasingly recognized as participants in regulating glycolytic metabolism, which has historically been regarded as the main metabolic pathway in intervertebral discs due to their avascular properties. Indeed, mitochondrial structural and functional disruption has been observed in degenerated nucleus pulposus (NP) cells and intervertebral discs. Multilevel and well-orchestrated strategies, namely, mitochondrial quality control (MQC), are involved in the maintenance of mitochondrial integrity, mitochondrial proteostasis, the mitochondrial antioxidant system, mitochondrial dynamics, mitophagy, and mitochondrial biogenesis. Here, we address the key evidence and current knowledge of the role of mitochondrial function in the IDD process and consider how MQC strategies contribute to the protective and detrimental properties of mitochondria in NP cell function. The relevant potential therapeutic treatments targeting MQC for IDD intervention are also summarized. Further clarification of the functional and synergistic mechanisms among MQC mechanisms may provide useful clues for use in developing novel IDD treatments.

참고문헌 (Reference)

1 Trout, J. J., "Ultrastructure of the human intervertebral disc. I. Changes in notochordal cells with age" 14 : 359-369, 1982

2 Melber, A., "UPR(mt)regulation and output : a stress response mediated by mitochondrial-nuclear communication" 28 : 281-295, 2018

3 Scarpulla, R. C., "Transcriptional integration of mitochondrial biogenesis" 23 : 459-466, 2012

4 Gogate, S. S., "Tonicity enhancer binding protein(TonEBP)and hypoxia-inducible factor(HIF)coordinate heat shock protein 70(Hsp70)expression in hypoxic nucleus pulposus cells : role of Hsp70 in HIF-1α degradation" 27 : 1106-1117, 2012

5 Smith, H. L., "The unfolded protein response : mechanisms and therapy of neurodegeneration" 139 : 2113-2121, 2016

6 Durcan, T. M., "The three ‘P’s of mitophagy : PARKIN, PINK1, and posttranslational modifications" 29 : 989-999, 2015

7 de Vries, S. A., "The stimulatory effect of notochordal cell-conditioned medium in a nucleus pulposus explant culture" 22 : 103-110, 2016

8 Hoppins, S., "The regulation of mitochondrial dynamics" 29 : 46-52, 2014

9 Ashrafi, G., "The pathways of mitophagy for quality control and clearance of mitochondria" 20 : 31-42, 2013

10 Kang, L., "The mitochondria-targeted anti-oxidant MitoQ protects against intervertebral disc degeneration by ameliorating mitochondrial dysfunction and redox imbalance" 53 : e12779-, 2020

11 Zhao, C. Q., "The cell biology of intervertebral disc aging and degeneration" 6 : 247-261, 2007

12 Wang, W., "Superoxide flashes in single mitochondria" 134 : 279-290, 2008

13 Fukai, T., "Superoxide dismutases : role in redox signaling, vascular function, and diseases" 15 : 1583-1606, 2011

14 Aldosari, S., "Subcellular reactive oxygen species(ROS)in cardiovascular pathophysiology" 7 : 14-, 2018

15 Knuppertz, L., "Stressdependent opposing roles for mitophagy in aging of the ascomycete Podospora anserina" 13 : 1037-1052, 2017

16 Kim, S., "Sphingosine kinase activates the mitochondrial unfolded protein response and is targeted to mitochondria by stress" 24 : 2932-2945, 2018

17 Rodrigues-Pinto, R., "Spatiotemporal analysis of putative notochordal cell markers reveals CD24 and keratins 8, 18, and 19 as notochord-specific markers during early human intervertebral disc development" 34 : 1327-1340, 2016

18 Jianle Wang, "Small molecule natural compound agonist of SIRT3 as a therapeutic target for the treatment of intervertebral disc degeneration" 생화학분자생물학회 50 : 1-14, 2018

19 Song, Y., "Sirtuin 3-dependent mitochondrial redox homeostasis protects against AGEs-induced intervertebral disc degeneration" 19 : 339-353, 2018

20 Naresh, N. U., "Signaling and regulation of the mitochondrial unfolded protein response" 11 : a033944-, 2019

21 Guehring, T., "Sensitivity of notochordal disc cells to mechanical loading : an experimental animal study" 19 : 113-121, 2010

22 Kenny, T. C., "Selected mitochondrial DNA landscapes activate the SIRT3 axis of the UPR(mt)to promote metastasis" 36 : 4393-4404, 2017

23 Wang, Y., "SIRT1 alleviates high-magnitude compression-induced senescence in nucleus pulposus cells via PINK1-dependent mitophagy" 12 : 16126-16141, 2020

24 Risbud, M. V., "Role of cytokines in intervertebral disc degeneration : pain and disc content" 10 : 44-56, 2014

25 Li, K., "Resveratrol protects against sodium nitroprusside induced nucleus pulposus cell apoptosis by scavenging ROS" 41 : 2485-2492, 2018

26 Kang, L., "Restoration of autophagic flux rescues oxidative damage and mitochondrial dysfunction to protect against intervertebral disc degeneration" 2019 : 7810320-, 2019

27 Trachootham, D., "Redox regulation of cell survival" 10 : 1343-1374, 2008

28 Miyazaki, S., "Recombinant human SIRT1 protects against nutrient deprivation-induced mitochondrial apoptosis through autophagy induction in human intervertebral disc nucleus pulposus cells" 17 : 253-, 2015

29 Cai, X., "ROS-mediated lysosomal membrane permeabilization is involved in bupivacaine-induced death of rabbit intervertebral disc cells" 18 : 65-76, 2018

30 Feng, C., "ROS : crucial intermediators in the pathogenesis of intervertebral disc degeneration" 2017 : 5601593-, 2017

31 Chen, J., "Protective effects of ginsenoside Rg3 on TNF-α-induced human nucleus pulposus cells through inhibiting NF-κB signaling pathway" 216 : 1-9, 2019

32 Xu, X., "Progerin accumulation in nucleus pulposus cells impairs mitochondrial function and induces intervertebral disc degeneration and therapeutic effects of sulforaphane" 9 : 2252-2267, 2019

33 Wang, J., "Polydatin suppresses nucleus pulposus cell senescence, promotes matrix homeostasis and attenuates intervertebral disc degeneration in rats" 22 : 5720-5731, 2018

34 Chu, H., "Plumbagin exerts protective effects in nucleus pulposus cells by attenuating hydrogen peroxide-induced oxidative stress, inflammation and apoptosis through NF-κB and Nrf-2" 37 : 1669-1676, 2016

35 Dong, Y., "Pilose antler peptide attenuates LPS-induced inflammatory reaction" 108 : 272-276, 2018

36 Andreux, P. A., "Pharmacological approaches to restore mitochondrial function" 12 : 465-483, 2013

37 Zhang, Z., "Parkin-mediated mitophagy as a potential therapeutic target for intervertebral disc degeneration" 9 : 980-, 2018

38 Urban, J. P., "Nutrition of the intervertebral disc" 29 : 2700-2709, 2004

39 Grunhagen, T., "Nutrient supply and intervertebral disc metabolism" 88 (88): 30-35, 2006

40 Liu, J., "Nutrient deprivation induces apoptosis of nucleus pulposus cells via activation of the BNIP3/AIF signalling pathway" 16 : 7253-7260, 2017

41 Jiao, S., "Nucleus pulposus cell apoptosis is attenuated by CDMP-2 through regulating oxidative damage under the hyperosmotic environment" 38 : BSR2018117-, 2018

42 Guehring, T., "Notochordal intervertebral disc cells : sensitivity to nutrient deprivation" 60 : 1026-1034, 2009

43 Erwin, W. M., "Notochordal cells protect nucleus pulposus cells from degradation and apoptosis : implications for the mechanisms of intervertebral disc degeneration" 13 : R215-, 2011

44 Mehrkens, A., "Notochordal cell-derived conditioned medium protects human nucleus pulposus cells from stress-induced apoptosis" 17 : 579-588, 2017

45 de Vries, S., "Notochordal cell matrix as a therapeutic agent for intervertebral disc regeneration" 25 : 830-841, 2019

46 Yurube, T., "Notochordal cell disappearance and modes of apoptotic cell death in a rat tail static compression-induced disc degeneration model" 16 : R31-, 2014

47 Yung, H. W., "Noncanonical mitochondrial unfolded protein response impairs placental oxidative phosphorylation in early-onset preeclampsia" 116 : 18109-18118, 2019

48 Rasool, S., "New insights into the structure of PINK1 and the mechanism of ubiquitin phosphorylation" 53 : 515-534, 2018

49 Gu, R., "Moracin attenuates LPS-induced inflammation in nucleus pulposus cells via Nrf2/HO-1 and NF-?B/TGF-á pathway" 39 : BSR2019167-, 2019

50 Apostolova, N., "Molecular strategies for targeting antioxidants to mitochondria : therapeutic implications" 22 : 686-729, 2015

51 Pickles, S., "Mitophagy and quality control mechanisms in mitochondrial maintenance" 28 : R170-r185, 2018

52 Seli, E., "Mitochondrial unfolded protein response : a stress response with implications for fertility and reproductive aging" 111 : 197-204, 2019

53 Murphy, M. P., "Mitochondrial thiols in antioxidant protection and redox signaling : distinct roles for glutathionylation and other thiol modifications" 16 : 476-495, 2012

54 Zhou, B., "Mitochondrial permeability uncouples elevated autophagy and lifespan extension" 177 : 299-314, 2019

55 Kroemer, G., "Mitochondrial membrane permeabilization in cell death" 87 : 99-163, 2007

56 Yao, C. H., "Mitochondrial fusion supports increased oxidative phosphorylation during cell proliferation" 8 : e41351-, 2019

57 Youle, R. J., "Mitochondrial fission, fusion, and stress" 337 : 1062-1065, 2012

58 Li, J., "Mitochondrial elongation-mediated glucose metabolism reprogramming is essential for tumour cell survival during energy stress" 36 : 4901-4912, 2017

59 Martin, J. A., "Mitochondrial electron transport and glycolysis are coupled in articular cartilage" 20 : 323-329, 2012

60 Wai, T., "Mitochondrial dynamics and metabolic regulation" 27 : 105-117, 2016

61 Whitaker, R. M., "Mitochondrial biogenesis as a pharmacological target : a new approach to acute and chronic diseases" 56 : 229-249, 2016

62 Bouchez, C., "Mitochondrial biogenesis and mitochondrial reactive oxygen species(ROS) : a complex relationship regulated by the cAMP/PKA signaling pathway" 8 : 287-, 2019

63 Dorn, G. W. 2nd, Vega, R. B., "Mitochondrial biogenesis and dynamics in the developing and diseased heart" 29 : 1981-1991, 2015

64 Ploumi, C., "Mitochondrial biogenesis and clearance : a balancing act" 284 : 183-195, 2017

65 Wen-Ning Xu, "Mitochondrial NDUFA4L2 attenuates the apoptosis of nucleus pulposus cells induced by oxidative stress via the inhibition of mitophagy" 생화학분자생물학회 51 : 1-16, 2019

66 McElroy, G. S., "Mitochondria control acute and chronic responses to hypoxia" 356 : 217-222, 2017

67 Chen, Y., "Mfn2 is involved in intervertebral disc degeneration through autophagy modulation" 28 : 363-374, 2020

68 Chen, D., "Metformin protects against apoptosis and senescence in nucleus pulposus cells and ameliorates disc degeneration in vivo" 7 : e2441-, 2016

69 Yang, L., "Metformin alleviates lead-induced mitochondrial fragmentation via AMPK/Nrf2 activation in SH-SY5Y cells" 36 : 101626-, 2020

70 Mahrouf-Yorgov, M., "Mesenchymal stem cells sense mitochondria released from damaged cells as danger signals to activate their rescue properties" 24 : 1224-1238, 2017

71 He, R., "Melatonin resists oxidative stress-induced apoptosis in nucleus pulposus cells" 199 : 122-130, 2018

72 Chen, Y., "Melatonin ameliorates intervertebral disc degeneration via the potential mechanisms of mitophagy induction and apoptosis inhibition" 23 : 2136-2148, 2019

73 Fernando, H. N., "Mechanical loading affects the energy metabolism of intervertebral disc cells" 29 : 1634-1641, 2011

74 Tsai, T. T., "MEK/ERK signaling controls osmoregulation of nucleus pulposus cells of the intervertebral disc by transactivation of TonEBP/OREBP" 22 : 965-974, 2007

75 Vlaeyen, J. W. S., "Low back pain" 4 : 52-, 2018

76 Pérez, M. J., "Loss of function of the mitochondrial peptidase PITRM1induces proteotoxic stress and Alzheimer’s disease-like pathology in human cerebral organoids" 2020

77 Merceron, C., "Loss of HIF-1α in the notochord results in cell death and complete disappearance of the nucleus pulposus" 9 : e110768-, 2014

78 Zhang, Y., "Listeria hijacks host mitophagy through a novel mitophagy receptor to evade killing" 20 : 433-446, 2019

79 Gan, J. C., "Intervertebral disc tissue engineering I : characterization of the nucleus pulposus" 411 : 305-314, 2003

80 Lv, F., "In search of nucleus pulposus-specific molecular markers" 53 : 600-610, 2014

81 Weiler, C., "Immunohistochemical identification of notochordal markers in cells in the aging human lumbar intervertebral disc" 19 : 1761-1770, 2010

82 Hua, W., "Icariin protects human nucleus pulposus cells from hydrogen peroxide-induced mitochondria-mediated apoptosis by activating nuclear factor erythroid 2-related factor 2" 1866 : 165575-, 2020

83 Madhu, V., "Hypoxic regulation of mitochondrial metabolism and mitophagy in nucleus pulposus cells is dependent on HIF-1α-BNIP3 axis" 35 : 1504-1524, 2020

84 Xu, D., "Hydrogen sulfide protects against endoplasmic reticulum stress and mitochondrial injury in nucleus pulposus cells and ameliorates intervertebral disc degeneration" 117 : 357-369, 2017

85 Zhao, L., "Hydrogen peroxide induces programmed necrosis in rat nucleus pulposus cells through the RIP1/RIP3-PARP-AIF pathway" 36 : 1269-1282, 2018

86 Tang, P., "Honokiol alleviates the degeneration of intervertebral disc via suppressing the activation of TXNIP-NLRP3 inflammasome signal pathway" 120 : 368-379, 2018

87 Park, E. Y., "High glucose-induced oxidative stress promotes autophagy through mitochondrial damage in rat notochordal cells" 37 : 2507-2514, 2013

88 Yi, W., "HO-1 overexpression alleviates senescence by inducing autophagy via the mitochondrial route in human nucleus pulposus cells" 2020 : 8402-8415, 2020

89 Collaborators GDaIIaP, "Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017" 392 : 1789-1858, 2018

90 Meachim, G., "Fine structure of juvenile human nucleus pulposus" 107 : 337-350, 1970

91 Lu, S., "Ferroportin-dependent iron homeostasis protects against oxidative stress-induced nucleus pulposus cell ferroptosis and ameliorates intervertebral disc degeneration in vivo" 2021 : 6670497-, 2021

92 Wright, D. C., "Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression" 282 : 194-199, 2007

93 Jin, L. Y., "Estradiol alleviates intervertebral disc degeneration through modulating the antioxidant enzymes and inhibiting autophagy in the model of menopause rats" 2018 : 7890291-, 2018

94 Won, H. Y., "Effect of hyperglycemia on apoptosis of notochordal cells and intervertebral disc degeneration in diabetic rats" 11 : 741-748, 2009

95 Prieto, J., "Early ERK1/2 activation promotes DRP1-dependent mitochondrial fission necessary for cell reprogramming" 7 : 11124-, 2016

96 Lin, H., "Drp1 mediates compression-induced programmed necrosis of rat nucleus pulposus cells by promoting mitochondrial translocation of p53 and nuclear translocation of AIF" 487 : 181-188, 2017

97 Lawson, L. Y., "Developmental mechanisms of intervertebral disc and vertebral column formation" 6 : e283-, 2017

98 Li, Z., "CsA attenuates compression-induced nucleus pulposus mesenchymal stem cells apoptosis via alleviating mitochondrial dysfunction and oxidative stress" 205 : 26-37, 2018

99 Chen, S., "Critical contribution of RIPK1 mediated mitochondrial dysfunction and oxidative stress to compression-induced rat nucleus pulposus cells necroptosis and apoptosis" 23 : 299-313, 2018

100 Palikaras, K., "Coupling mitogenesis and mitophagy for longevity" 11 : 1428-1430, 2015

101 Palikaras, K., "Coordination of mitophagy and mitochondrial biogenesis during ageing in C. elegans" 521 : 525-528, 2015

102 de Vries, S. A., "Conditioned medium derived from notochordal cell-rich nucleus pulposus tissue stimulates matrix production by canine nucleus pulposus cells and bone marrow-derived stromal cells" 21 : 1077-1084, 2015

103 Huang, D., "Compression-induced senescence of nucleus pulposus cells by promoting mitophagy activation via the PINK1/PARKIN pathway" 24 : 5850-5864, 2020

104 Chooi, W. H., "Compression loading-induced stress responses in intervertebral disc cells encapsulated in 3D collagen constructs" 6 : 26449-, 2016

105 Chooi, W. H., "Compression loading induced cellular stress response of intervertebral disc cells in organ culture" 6 : 2016

106 Xie, L., "CircERCC2 ameliorated intervertebral disc degeneration by regulating mitophagy and apoptosis through miR-182-5p/SIRT1 axis" 10 : 751-, 2019

107 Sentelle, R. D., "Ceramide targets autophagosomes to mitochondria and induces lethal mitophagy" 8 : 831-838, 2012

108 Martin, S. J., "Cell biology. Opening the cellular poison cabinet" 330 : 1330-1331, 2010

109 Gatica, D., "Cargo recognition and degradation by selective autophagy" 20 : 233-242, 2018

110 Chu, C. T., "Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells" 15 : 1197-1205, 2013

111 Görlach, A., "Calcium and ROS : a mutual interplay" 6 : 260-271, 2015

112 Liu, Y., "Caenorhabditis elegans pathways that surveil and defend mitochondria" 508 : 406-410, 2014

113 Deyo, R. A., "CLINICAL PRACTICE. Herniated Lumbar Intervertebral Disk" 374 : 1763-1772, 2016

114 Roughley, P. J., "Biology of intervertebral disc aging and degeneration : involvement of the extracellular matrix" 29 : 2691-2699, 2004

115 Silagi, E. S., "Bicarbonate recycling by HIF-1-dependent carbonic anhydrase isoforms 9 and 12 is critical in maintaining intracellular pH and viability of nucleus pulposus cells" 33 : 338-355, 2018

116 Kale, J., "BCL-2 family proteins : changing partners in the dance towards death" 25 : 65-80, 2018

117 Liu, Y., "Aspirin-mediated attenuation of intervertebral disc degeneration by ameliorating reactive oxygen species in vivo and in vitro" 2019 : 7189854-, 2019

118 Amartuvshin, O., "Aging shifts mitochondrial dynamics toward fission to promote germline stem cell loss" 19 : e13191-, 2020

119 Hartman, R., "Age-dependent changes in intervertebral disc cell mitochondria and bioenergetics" 36 : 171-183, 2018

120 Song, Y., "Advanced glycation end products regulate anabolic and catabolic activities via NLRP3-inflammasome activation in human nucleus pulposus cells" 21 : 1373-1387, 2017

121 Jiang, L. B., "Activation of autophagy via Ca(2+)-dependent AMPK/mTOR pathway in rat notochordal cells is a cellular adaptation under hyperosmotic stress" 14 : 867-879, 2015

122 Zhao, K., "Acid-sensing ion channels regulate nucleus pulposus cell inflammation and pyroptosis via the NLRP3 inflammasome in intervertebral disc degeneration" 54 : e12941-, 2021

123 Acin-Perez, R., "Ablation of the stress protease OMA1 protects against heart failure in mice" 10 : 2018

124 Hirata, H., "A rat tail temporary static compression model reproduces different stages of intervertebral disc degeneration with decreased notochordal cell phenotype" 32 : 455-463, 2014

125 Kirkin, V., "A diversity of selective autophagy receptors determines the specificity of the autophagy pathway" 76 : 268-285, 2019

126 Shirihai, O. S., "2nd How mitochondrial dynamism orchestrates mitophagy" 116 : 1835-1849, 2015

127 Gustafsson, Å. B., "2nd Evolving and expanding the roles of mitophagy as a homeostatic and pathogenic process" 99 : 853-892, 2019

128 Bai, X. D., "(*)Coculture with partial digestion notochordal cell-rich nucleus pulposus tissue activates degenerative human nucleus pulposus cells" 23 : 837-846, 2017