质膜的损伤修复及相关模型
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摘要
生物膜的磷脂双分子层将细胞与外界环境分开。大部分细胞会在机械损伤或化学应激下引发质膜损伤,如果不及时修复将会导致细胞死亡。胞外钙离子通过伤口进入细胞,作为损伤的最初信号,会诱发一系列的修复反应。随后,胞内细胞器也释放钙离子,并产生系列细胞行为来应对损伤,维护质膜的完整性。本文介绍了在损伤修复过程的胞吞作用、胞吐作用、胞外小泡脱落等细胞行为。综述了补丁模型、修复帽模型和大损伤修复的模型特点。补丁模型是最早的修复模型,提出后不断得到完善。细胞除了需要在损伤处聚集小泡、融合形成补丁外,还需通过胞吐、胞吞和出芽(小泡脱落)等方式参与伤口修复。本文简要介绍参与质膜修复的重要蛋白质如钙蛋白酶、dysferlin、MG53、膜联蛋白、突触结合蛋白(Syt-VⅡ)、ESCRTⅢ、酸性鞘磷脂酶、细胞骨架蛋白质等在修复过程中的作用。
Eukaryotic cells from extracellular environments are separated by plasma membranes composed of phospholipid bilayers. Most cells are subject to mechanical or chemical stresses that could disrupt the plasma membrane. If these disruptions are not closed rapidly,it may lead to the cell deaths.As a result,cells have evolved active strategies to mend the broken membranes. A series of repair responses would be induced by extracellular calcium ions to enter cells through lesions as a primary signal. Then,intracellular calcium ions were released from intracellular organelles. A number of proteins were recruited to deal with the damage and maintain the integrity of the plasma membrane. This article introduces cell behaviors including the endocytosis,exocytosis,budding/blebbing,and reviewed the patch model,the repairing cap model,and the large wounds repairing. The patch model is the earliest repair model,and has been revised continuously. The wound repair process needs vesicles aggregation,vesicle fusion to form patches, and also via exocytosis, endocytosis and blebbing of extracellular vesicles. We will also introduce proteins related to membrane repair,including calpain,dysferlin,MG53,annexins,Syt-VⅡ,ESCRT-Ⅲ,acidic sphingomyelinase and cytoskeleton protein.
Eukaryotic cells from extracellular environments are separated by plasma membranes composed of phospholipid bilayers. Most cells are subject to mechanical or chemical stresses that could disrupt the plasma membrane. If these disruptions are not closed rapidly,it may lead to the cell deaths.As a result,cells have evolved active strategies to mend the broken membranes. A series of repair responses would be induced by extracellular calcium ions to enter cells through lesions as a primary signal. Then,intracellular calcium ions were released from intracellular organelles. A number of proteins were recruited to deal with the damage and maintain the integrity of the plasma membrane. This article introduces cell behaviors including the endocytosis,exocytosis,budding/blebbing,and reviewed the patch model,the repairing cap model,and the large wounds repairing. The patch model is the earliest repair model,and has been revised continuously. The wound repair process needs vesicles aggregation,vesicle fusion to form patches, and also via exocytosis, endocytosis and blebbing of extracellular vesicles. We will also introduce proteins related to membrane repair,including calpain,dysferlin,MG53,annexins,Syt-VⅡ,ESCRT-Ⅲ,acidic sphingomyelinase and cytoskeleton protein.
引文
[1] Cheng X,Zhang X,Yu L,et al. Calcium signaling in membrane repair[J]. Semin Cell Dev Biol,2015,45:24-31
[2] Andrews NW,Corrotte M,Castro-Gomes T. Above the fray:surface remodeling by secreted lysosomal enzymes leads to endocytosis-mediated plasma membrane repair[J]. Semin Cell Dev Biol,2015,45:10-17
[3] Prins D,Michalak M. Organellar calcium buffers[J]. Cold Spring Harb Perspect Biol,2011,3(3). pii:a004069
[4] Idone V,Tam C,Goss JW,et al. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis[J]. J Cell Biol,2008,180(5):905-914
[5] Steinhardt RA,Bi G,Alderton JM. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release[J].Science,1994,263(5145):390-393
[6]赵凯,卫涛涛.溶酶体与细胞凋亡[J].生命科学(Zhao K,Wei TT. Lysosome and apoptosis[J]. Chin Bull Life Sci),2011,23(11):1063-1068
[7] Bonifacino JS,Glick BS. The mechanisms of vesicle budding and fusion[J]. Cell,2004,116(2):153-166
[8] Togo T,Steinhardt RA. Nonmuscle myosin IIA and IIB have distinct functions in the exocytosis-dependent process of cell membrane repair[J]. Mol Biol Cell,2004,15(2):688-695
[9] Vieira OV. Rab3a and Rab10 are regulators of lysosome exocytosis and plasma membrane repair[J]. Small GTPases,2018,9(4):349-351
[10] Mc Neil PL,Kirchhausen T. An emergency response team for membrane repair[J]. Nat Rev Mol Cell Biol,2005,6(6):499-505
[11] Rao SK,Huynh C,Proux-Gillardeaux V,et al. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis[J]. J Biol Chem,2004,279(19):20471-20479
[12] Jaiswal JK, Andrews NW, Simon SM. Membrane proximal lysosomes are the major vesicles responsible for calciumdependent exocytosis in nonsecretory cells[J]. J Cell Biol,2002,159(4):625-635
[13] Pang ZP,Sudhof TC. Cell biology of Ca2+-triggered exocytosis[J]. Curr Opin Cell Biol,2010,22(4):496-505
[14] Geppert M,Goda Y,Stevens CF,et al. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion[J].Nature,1997,387(6635):810-814
[15] Encarna92o M,Espada L,Escrevente C,et al. A Rab3adependent complex essential for lysosome positioning and plasma membrane repair[J]. J Cell Biol,2016,213(6):631-640
[16] Lariccia V,Fine M,Magi S,et al. Massive calcium-activated endocytosis without involvement of classical endocytic proteins[J]. J Gen Physiol,2011,137(1):111-132
[17] Liu P,Anderson RG. Compartmentalized production of ceramide at the cell surface[J]. J Biol Chem, 1995, 270(45):27179-27185
[18] Lajoie P,Nabi IR. Lipid rafts,caveolae,and their endocytosis[J]. Int Rev Cell Mol Biol,2010,282:135-163
[19] Defour A, Van der Meulen JH, Bhat R, et al. Dysferlin regulates cell membrane repair by facilitating injury triggered acid sphingomyelinase secretion[J]. Cell Death Dis,2014,5:e1306
[20] Tam C, Idone V, Devlin C, et al. Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair[J]. J Cell Biol,2010,189(6):1027-1038
[21] Andrews NW, Almeida PE, Corrotte M. Damage control:cellular mechanisms of plasma membrane repair[J]. Trends Cell Biol,2014,24(12):734-742
[22] Kovtun O,Tillu VA,Ariotti N,et al. Cavin family proteins and the assembly of caveolae[J]. J Cell Sci,2015,128(7):1269-1278
[23] Cai C,Weisleder N,Ko JK,et al. Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53,caveolin-3,and dysferlin[J]. J Biol Chem,2009,284(23):15894-15902
[24] Jimenez AJ, Maiuri P, Lafaurie-Janvore J, et al. ESCRT machinery is required for plasma membrane repair[J]. Science,2014,343(6174):1247136
[25] Saksena S,Sun J,Chu T,et al. ESCRTing proteins in the endocytic pathway[J]. Trends Biochem Sci,2007,32(12):561-573
[26] Mc Neil PL. Repairing a torn cell surface:make way,lysosomes to the rescue[J]. J Cell Sci,2002,115(Pt 5):873-879
[27] Davenport NR,Sonnemann KJ,Eliceiri KW,et al. Membrane dynamics during cellular wound repair[J]. Mol Biol Cell,2016,27(14):2272-2285
[28] Bansal D,Miyake K,Vogel SS,et al. Defective membrane repair in dysferlin-deficient muscular dystrophy[J]. Nature,2003,423(6936):168-172
[29] Han R,Campbell KP. Dysferlin and muscle membrane repair[J]. Curr Opin Cell Biol,2007,19(4):409-416
[30] Redpath GM,Woolger N,Piper AK,et al. Calpain cleavage within dysferlin exon 40a releases a synaptotagmin-like module for membrane repair[J]. Mol Biol Cell,2014,25(19):3037-3048
[31] Ahn MK,Lee KJ,Cai C,et al. Mitsugumin 53 regulates extracellular Ca2+entry and intracellular Ca2+release via Orai1and RyR1 in skeletal muscle[J]. Sci Rep,2016,6:36909
[32] Cooper ST,Mc Neil PL. Membrane repair:mechanisms and pathophysiology[J]. Physiol Rev,2015,95(4):1205-1240
[33] Blazek AD,Paleo BJ,Weisleder N. Plasma membrane repair:a central process for maintaining cellular homeostasis[J].Physiology(Bethesda),2015,30(6):438-448
[34] Lennon NJ,Kho A,Bacskai BJ,et al. Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing[J]. J Biol Chem,2003,278(50):50466-50473
[35] Demonbreun AR,Quattrocelli M,Barefield DY,et al. An actindependent annexin complex mediates plasma membrane repair in muscle[J]. J Cell Biol,2016,213(6):705-718
[36] Wang X,Yin H,Zhang H,et al. NF-κB-driven improvement of EHD1 contributes to erlotinib resistance in EGFR-mutant lung cancers[J]. Cell Death Dis,2018,9(4):418
[37] Bouter A,Carmeille R,Gounou C,et al. Review:Annexin-A5and cell membrane repair[J]. Placenta,2015,36 Suppl 1:S43-49
[38] Swaggart KA,Demonbreun AR,Vo AH,et al. Annexin A6modifies muscular dystrophy by mediating sarcolemmal repair[J]. Proc Natl AcadSci U S A,2014,111(16):6004-6009
[39] Boye TL,Maeda K,Pezeshkian W,et al. Annexin A4 and A6induce membrane curvature and constriction during cell membrane repair[J]. Nat Commun,2017,8(1):1623
[40] Mc Dade JR,Michele DE. Membrane damage-induced vesiclevesicle fusion of dysferlin-containing vesicles in muscle cells requires microtubules and kinesin[J]. Hum Mol Genet,2014,23(7):1677-1686
[2] Andrews NW,Corrotte M,Castro-Gomes T. Above the fray:surface remodeling by secreted lysosomal enzymes leads to endocytosis-mediated plasma membrane repair[J]. Semin Cell Dev Biol,2015,45:10-17
[3] Prins D,Michalak M. Organellar calcium buffers[J]. Cold Spring Harb Perspect Biol,2011,3(3). pii:a004069
[4] Idone V,Tam C,Goss JW,et al. Repair of injured plasma membrane by rapid Ca2+-dependent endocytosis[J]. J Cell Biol,2008,180(5):905-914
[5] Steinhardt RA,Bi G,Alderton JM. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release[J].Science,1994,263(5145):390-393
[6]赵凯,卫涛涛.溶酶体与细胞凋亡[J].生命科学(Zhao K,Wei TT. Lysosome and apoptosis[J]. Chin Bull Life Sci),2011,23(11):1063-1068
[7] Bonifacino JS,Glick BS. The mechanisms of vesicle budding and fusion[J]. Cell,2004,116(2):153-166
[8] Togo T,Steinhardt RA. Nonmuscle myosin IIA and IIB have distinct functions in the exocytosis-dependent process of cell membrane repair[J]. Mol Biol Cell,2004,15(2):688-695
[9] Vieira OV. Rab3a and Rab10 are regulators of lysosome exocytosis and plasma membrane repair[J]. Small GTPases,2018,9(4):349-351
[10] Mc Neil PL,Kirchhausen T. An emergency response team for membrane repair[J]. Nat Rev Mol Cell Biol,2005,6(6):499-505
[11] Rao SK,Huynh C,Proux-Gillardeaux V,et al. Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis[J]. J Biol Chem,2004,279(19):20471-20479
[12] Jaiswal JK, Andrews NW, Simon SM. Membrane proximal lysosomes are the major vesicles responsible for calciumdependent exocytosis in nonsecretory cells[J]. J Cell Biol,2002,159(4):625-635
[13] Pang ZP,Sudhof TC. Cell biology of Ca2+-triggered exocytosis[J]. Curr Opin Cell Biol,2010,22(4):496-505
[14] Geppert M,Goda Y,Stevens CF,et al. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion[J].Nature,1997,387(6635):810-814
[15] Encarna92o M,Espada L,Escrevente C,et al. A Rab3adependent complex essential for lysosome positioning and plasma membrane repair[J]. J Cell Biol,2016,213(6):631-640
[16] Lariccia V,Fine M,Magi S,et al. Massive calcium-activated endocytosis without involvement of classical endocytic proteins[J]. J Gen Physiol,2011,137(1):111-132
[17] Liu P,Anderson RG. Compartmentalized production of ceramide at the cell surface[J]. J Biol Chem, 1995, 270(45):27179-27185
[18] Lajoie P,Nabi IR. Lipid rafts,caveolae,and their endocytosis[J]. Int Rev Cell Mol Biol,2010,282:135-163
[19] Defour A, Van der Meulen JH, Bhat R, et al. Dysferlin regulates cell membrane repair by facilitating injury triggered acid sphingomyelinase secretion[J]. Cell Death Dis,2014,5:e1306
[20] Tam C, Idone V, Devlin C, et al. Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair[J]. J Cell Biol,2010,189(6):1027-1038
[21] Andrews NW, Almeida PE, Corrotte M. Damage control:cellular mechanisms of plasma membrane repair[J]. Trends Cell Biol,2014,24(12):734-742
[22] Kovtun O,Tillu VA,Ariotti N,et al. Cavin family proteins and the assembly of caveolae[J]. J Cell Sci,2015,128(7):1269-1278
[23] Cai C,Weisleder N,Ko JK,et al. Membrane repair defects in muscular dystrophy are linked to altered interaction between MG53,caveolin-3,and dysferlin[J]. J Biol Chem,2009,284(23):15894-15902
[24] Jimenez AJ, Maiuri P, Lafaurie-Janvore J, et al. ESCRT machinery is required for plasma membrane repair[J]. Science,2014,343(6174):1247136
[25] Saksena S,Sun J,Chu T,et al. ESCRTing proteins in the endocytic pathway[J]. Trends Biochem Sci,2007,32(12):561-573
[26] Mc Neil PL. Repairing a torn cell surface:make way,lysosomes to the rescue[J]. J Cell Sci,2002,115(Pt 5):873-879
[27] Davenport NR,Sonnemann KJ,Eliceiri KW,et al. Membrane dynamics during cellular wound repair[J]. Mol Biol Cell,2016,27(14):2272-2285
[28] Bansal D,Miyake K,Vogel SS,et al. Defective membrane repair in dysferlin-deficient muscular dystrophy[J]. Nature,2003,423(6936):168-172
[29] Han R,Campbell KP. Dysferlin and muscle membrane repair[J]. Curr Opin Cell Biol,2007,19(4):409-416
[30] Redpath GM,Woolger N,Piper AK,et al. Calpain cleavage within dysferlin exon 40a releases a synaptotagmin-like module for membrane repair[J]. Mol Biol Cell,2014,25(19):3037-3048
[31] Ahn MK,Lee KJ,Cai C,et al. Mitsugumin 53 regulates extracellular Ca2+entry and intracellular Ca2+release via Orai1and RyR1 in skeletal muscle[J]. Sci Rep,2016,6:36909
[32] Cooper ST,Mc Neil PL. Membrane repair:mechanisms and pathophysiology[J]. Physiol Rev,2015,95(4):1205-1240
[33] Blazek AD,Paleo BJ,Weisleder N. Plasma membrane repair:a central process for maintaining cellular homeostasis[J].Physiology(Bethesda),2015,30(6):438-448
[34] Lennon NJ,Kho A,Bacskai BJ,et al. Dysferlin interacts with annexins A1 and A2 and mediates sarcolemmal wound-healing[J]. J Biol Chem,2003,278(50):50466-50473
[35] Demonbreun AR,Quattrocelli M,Barefield DY,et al. An actindependent annexin complex mediates plasma membrane repair in muscle[J]. J Cell Biol,2016,213(6):705-718
[36] Wang X,Yin H,Zhang H,et al. NF-κB-driven improvement of EHD1 contributes to erlotinib resistance in EGFR-mutant lung cancers[J]. Cell Death Dis,2018,9(4):418
[37] Bouter A,Carmeille R,Gounou C,et al. Review:Annexin-A5and cell membrane repair[J]. Placenta,2015,36 Suppl 1:S43-49
[38] Swaggart KA,Demonbreun AR,Vo AH,et al. Annexin A6modifies muscular dystrophy by mediating sarcolemmal repair[J]. Proc Natl AcadSci U S A,2014,111(16):6004-6009
[39] Boye TL,Maeda K,Pezeshkian W,et al. Annexin A4 and A6induce membrane curvature and constriction during cell membrane repair[J]. Nat Commun,2017,8(1):1623
[40] Mc Dade JR,Michele DE. Membrane damage-induced vesiclevesicle fusion of dysferlin-containing vesicles in muscle cells requires microtubules and kinesin[J]. Hum Mol Genet,2014,23(7):1677-1686