Nicotinamide Phosphoribosyltransferase in Smooth Muscle Cells Maintains Genome Integrity, Resists Aortic Medial Degeneration, and Is Suppressed in Human Thoracic Aortic Aneurysm Disease

Circulation Research

Volumn 120, Issue 12, 2017, Pages 1889-1902

  Watson, Alanna ^a,b   Nong, Zengxuan ^a   Yin, Hao ^a   O'Neil, Caroline ^a   Fox, Stephanie ^b   Balint, Brittany ^b   Guo, Linrui ^b   Leo, Oberdan ^c   Chu, Michael W A ^b   Gros, Robert ^a   Pickering, J Geoffrey ^a,b  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

aortic disease; cell aging; DNA damage; extracellular matrix

Indexed keywords

ANGIOTENSIN II; BETA GALACTOSIDASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; NICOTINAMIDE RIBOSIDE; PROTEIN P16; CYTOKINE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE, HUMAN; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE, MOUSE;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTIC DISSECTION; AORTIC MEDIA; ARTICLE; ASCENDING AORTA; CELL DEGENERATION; CLINICAL ARTICLE; CONTROL SYSTEM; CONTROLLED STUDY; DNA DAMAGE; DNA STRAND BREAKAGE; ENZYME ACTIVITY; ENZYME DEFICIENCY; GENE REPRESSION; GENETIC SUSCEPTIBILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MOUSE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE DEFICIENCY; NONHUMAN; PREMATURITY; PRIORITY JOURNAL; SENESCENCE; SMOOTH MUSCLE CELL; THORACIC AORTA ANEURYSM; UPREGULATION; ANIMAL; AORTA; BIOSYNTHESIS; CELL CULTURE; DEFICIENCY; ENZYMOLOGY; FEMALE; GENETICS; GENOME; LASER CAPTURE MICRODISSECTION; MALE; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PROCEDURES; TUNICA MEDIA;

ADULT; AGED; ANIMALS; AORTA; AORTIC ANEURYSM, THORACIC; CELLS, CULTURED; CYTOKINES; DNA DAMAGE; FEMALE; GENOME; HUMANS; LASER CAPTURE MICRODISSECTION; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; MYOCYTES, SMOOTH MUSCLE; NICOTINAMIDE PHOSPHORIBOSYLTRANSFERASE; TUNICA MEDIA;

EID: 85016950162     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.310022     Document Type: Article

References (45)

1. Schlatmann TJ, Becker AE. Histologic changes in the normal aging aorta: implications for dissecting aortic aneurysm. Am J Cardiol. 1977; 39: 13-20.
2. Howard DP, Banerjee A, Fairhead JF, Perkins J, Silver LE, Rothwell PM; Oxford Vascular Study. Population-based study of incidence and outcome of acute aortic dissection and premorbid risk factor control: 10-year results from the Oxford Vascular Study. Circulation. 2013; 127: 2031-2037. doi: 10. 1161/CIRCULATIONAHA. 112. 000483.
3. Milewicz DM, Guo DC, Tran-Fadulu V, Lafont AL, Papke CL, Inamoto S, Kwartler CS, Pannu H. Genetic basis of thoracic aortic aneurysms and dissections: focus on smooth muscle cell contractile dysfunction. Annu Rev Genomics Hum Genet. 2008; 9: 283-302. doi: 10. 1146/annurev. genom. 8. 080706. 092303.
4. Li S, Van Den Diepstraten C, D'Souza SJ, Chan BM, Pickering JG. Vascular smooth muscle cells orchestrate the assembly of type I collagen via alpha2beta1 integrin, RhoA, and fibronectin polymerization. Am J Pathol. 2003; 163: 1045-1056.
5. Humphrey JD, Milewicz DM, Tellides G, Schwartz MA. Cell biology. Dysfunctional mechanosensing in aneurysms. Science. 2014; 344: 477-479. doi: 10. 1126/science. 1253026.
6. Ruiz-Torres A, Gimeno A, Melón J, Mendez L, Muñoz FJ, Macía M. Agerelated loss of proliferative activity of human vascular smooth muscle cells in culture. Mech Ageing Dev. 1999; 110: 49-55.
7. van der Veer E, Ho C, O'Neil C, Barbosa N, Scott R, Cregan SP, Pickering JG. Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J Biol Chem. 2007; 282: 10841-10845. doi: 10. 1074/jbc. C700018200.
8. Halushka MK, Angelini A, Bartoloni G, et al. Consensus statement on surgical pathology of the aorta from the Society for Cardiovascular Pathology and the Association For European Cardiovascular Pathology: II. Noninflammatory degenerative diseases-nomenclature and diagnostic criteria. Cardiovasc Pathol. 2016; 25: 247-257. doi: 10. 1016/j. carpath. 2016. 03. 002.
9. Dantzer F, Amé JC, Schreiber V, Nakamura J, Ménissier-de Murcia J, de Murcia G. Poly(ADP-ribose) polymerase-1 activation during DNA damage and repair. Methods Enzymol. 2006; 409: 493-510. doi: 10. 1016/ S0076-6879(05)09029-4.
10. Nikiforov A, Kulikova V, Ziegler M. The human NAD metabolome: functions, metabolism and compartmentalization. Crit Rev Biochem Mol Biol. 2015; 50: 284-297. doi: 10. 3109/10409238. 2015. 1028612.
11. Cantó C, Menzies KJ, Auwerx J. NAD(+) metabolism and the control of energy homeostasis: a balancing act between mitochondria and the nucleus. Cell Metab. 2015; 22: 31-53. doi: 10. 1016/j. cmet. 2015. 05. 023.
12. van der Veer E, Nong Z, O'Neil C, Urquhart B, Freeman D, Pickering JG. Pre-B-cell colony-enhancing factor regulates NAD+-dependent protein deacetylase activity and promotes vascular smooth muscle cell maturation. Circ Res. 2005; 97: 25-34. doi: 10. 1161/01. RES. 0000173298. 38808. 27.
13. Revollo JR, Körner A, Mills KF, Satoh A, Wang T, Garten A, Dasgupta B, Sasaki Y, Wolberger C, Townsend RR, Milbrandt J, Kiess W, Imai S. Nampt/PBEF/Visfatin regulates insulin secretion in beta cells as a systemic NAD biosynthetic enzyme. Cell Metab. 2007; 6: 363-375. doi: 10. 1016/j. cmet. 2007. 09. 003.
14. Zhou CC, Yang X, Hua X, Liu J, Fan MB, Li GQ, Song J, Xu TY, Li ZY, Guan YF, Wang P, Miao CY. Hepatic NAD(+) deficiency as a therapeutic target for non-alcoholic fatty liver disease in ageing. Br J Pharmacol. 2016; 173: 2352-2368. doi: 10. 1111/bph. 13513.
15. Frederick DW, Loro E, Liu L, et al. Loss of NAD homeostasis leads to progressive and reversible degeneration of skeletal muscle. Cell Metab. 2016; 24: 269-282. doi: 10. 1016/j. cmet. 2016. 07. 005.
16. Stein LR, Imai S. Specific ablation of Nampt in adult neural stem cells recapitulates their functional defects during aging. EMBO J. 2014; 33: 1321-1340. doi: 10. 1002/embj. 201386917.
17. Yin H, van der Veer E, Frontini MJ, Thibert V, O'Neil C, Watson A, Szasz P, Chu MW, Pickering JG. Intrinsic directionality of migrating vascular smooth muscle cells is regulated by NAD(+) biosynthesis. J Cell Sci. 2012; 125: 5770-5780. doi: 10. 1242/jcs. 110262.
18. Wang P, Li WL, Liu JM, Miao CY. NAMPT and NAMPT-controlled NAD metabolism in vascular repair. J Cardiovasc Pharmacol. 2016; 67: 474-481. doi: 10. 1097/FJC. 0000000000000332.
19. Wang P, Xu TY, Guan YF, Su DF, Fan GR, Miao CY. Perivascular adipose tissue-derived visfatin is a vascular smooth muscle cell growth factor: role of nicotinamide mononucleotide. Cardiovasc Res. 2009; 81: 370-380. doi: 10. 1093/cvr/cvn288.
20. de Picciotto NE, Gano LB, Johnson LC, Martens CR, Sindler AL, Mills KF, Imai S, Seals DR. Nicotinamide mononucleotide supplementation reverses vascular dysfunction and oxidative stress with aging in mice. Aging Cell. 2016; 15: 522-530. doi: 10. 1111/acel. 12461.
21. Rongvaux A, Galli M, Denanglaire S, Van Gool F, Drèze PL, Szpirer C, Bureau F, Andris F, Leo O. Nicotinamide phosphoribosyl transferase/ pre-B cell colony-enhancing factor/visfatin is required for lymphocyte development and cellular resistance to genotoxic stress. J Immunol. 2008; 181: 4685-4695.
22. Xin HB, Deng KY, Rishniw M, Ji G, Kotlikoff MI. Smooth muscle expression of Cre recombinase and eGFP in transgenic mice. Physiol Genomics. 2002; 10: 211-215. doi: 10. 1152/physiolgenomics. 00054. 2002.
23. Rateri DL, Davis FM, Balakrishnan A, Howatt DA, Moorleghen JJ, O'Connor WN, Charnigo R, Cassis LA, Daugherty A. Angiotensin II induces region-specific medial disruption during evolution of ascending aortic aneurysms. Am J Pathol. 2014; 184: 2586-2595. doi: 10. 1016/j. ajpath. 2014. 05. 014.
24. Owens AP 3rd, Subramanian V, Moorleghen JJ, Guo Z, McNamara CA, Cassis LA, Daugherty A. Angiotensin II induces a region-specific hyperplasia of the ascending aorta through regulation of inhibitor of differentiation 3. Circ Res. 2010; 106: 611-619. doi: 10. 1161/CIRCRESAHA. 109. 212837.
25. Vafaie F, Yin H, O'Neil C, Nong Z, Watson A, Arpino JM, Chu MW, Wayne Holdsworth D, Gros R, Pickering JG. Collagenase-resistant collagen promotes mouse aging and vascular cell senescence. Aging Cell. 2014; 13: 121-130. doi: 10. 1111/acel. 12155.
26. Yin H, Pickering JG. Cellular senescence and vascular disease: novel routes to better understanding and therapy. Can J Cardiol. 2016; 32: 612-623. doi: 10. 1016/j. cjca. 2016. 02. 051.
27. d'Adda di Fagagna F. Living on a break: cellular senescence as a DNAdamage response. Nat Rev Cancer. 2008; 8: 512-522
28. Gray K, Kumar S, Figg N, Harrison J, Baker L, Mercer J, Littlewood T, Bennett M. Effects of DNA damage in smooth muscle cells in atherosclerosis. Circ Res. 2015; 116: 816-826. doi: 10. 1161/ CIRCRESAHA. 116. 304921.
29. Gomez D, Kessler K, Michel JB, Vranckx R. Modifications of chromatin dynamics control Smad2 pathway activation in aneurysmal smooth muscle cells. Circ Res. 2013; 113: 881-890. doi: 10. 1161/ CIRCRESAHA. 113. 301989.
30. Kunieda T, Minamino T, Nishi J, Tateno K, Oyama T, Katsuno T, Miyauchi H, Orimo M, Okada S, Takamura M, Nagai T, Kaneko S, Komuro I. Angiotensin II induces premature senescence of vascular smooth muscle cells and accelerates the development of atherosclerosis via a p21-dependent pathway. Circulation. 2006; 114: 953-960. doi: 10. 1161/CIRCULATIONAHA. 106. 626606.
31. Matthews C, Gorenne I, Scott S, Figg N, Kirkpatrick P, Ritchie A, Goddard M, Bennett M. Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res. 2006; 99: 156-164. doi: 10. 1161/01. RES. 0000233315. 38086. bc.
32. Liu Y, Drozdov I, Shroff R, Beltran LE, Shanahan CM. Prelamin A accelerates vascular calcification via activation of the DNA damage response and senescence-associated secretory phenotype in vascular smooth muscle cells. Circ Res. 2013; 112: e99-109. doi: 10. 1161/ CIRCRESAHA. 111. 300543.
33. Rai P, Onder TT, Young JJ, McFaline JL, Pang B, Dedon PC, Weinberg RA. Continuous elimination of oxidized nucleotides is necessary to prevent rapid onset of cellular senescence. Proc Natl Acad Sci USA. 2009; 106: 169-174. doi: 10. 1073/pnas. 0809834106.
34. Nassour J, Martien S, Martin N, Deruy E, Tomellini E, Malaquin N, Bouali F, Sabatier L, Wernert N, Pinte S, Gilson E, Pourtier A, Pluquet O, Abbadie C. Defective DNA single-strand break repair is responsible for senescence and neoplastic escape of epithelial cells. Nat Commun. 2016; 7: 10399. doi: 10. 1038/ncomms10399.
35. Kuzminov A. Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc Natl Acad Sci USA. 2001; 98: 8241-8246. doi: 10. 1073/pnas. 131009198.
36. Beck C, Robert I, Reina-San-Martin B, Schreiber V, Dantzer F. Poly(ADPribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp Cell Res. 2014; 329: 18-25. doi: 10. 1016/j. yexcr. 2014. 07. 003.
37. Wang M, Wu W, Wu W, Rosidi B, Zhang L, Wang H, Iliakis G. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res. 2006; 34: 6170-6182. doi: 10. 1093/ nar/gkl840.
38. Noren Hooten N, Kompaniez K, Barnes J, Lohani A, Evans MK. Poly(ADP-ribose) polymerase 1 (PARP-1) binds to 8-oxoguanine-DNA glycosylase (OGG1). J Biol Chem. 2011; 286: 44679-44690. doi: 10. 1074/ jbc. M111. 255869.
39. Fisher AE, Hochegger H, Takeda S, Caldecott KW. Poly(ADP-ribose) polymerase 1 accelerates single-strand break repair in concert with poly(ADP-ribose) glycohydrolase. Mol Cell Biol. 2007; 27: 5597-5605. doi: 10. 1128/MCB. 02248-06.
40. Ho C, van der Veer E, Akawi O, Pickering JG. SIRT1 markedly extends replicative lifespan if the NAD+ salvage pathway is enhanced. FEBS Lett. 2009; 583: 3081-3085. doi: 10. 1016/j. febslet. 2009. 08. 031.
41. Chen HZ, Wang F, Gao P, et al. Age-associated sirtuin 1 reduction in vascular smooth muscle links vascular senescence and inflammation to abdominal aortic aneurysm. Circ Res. 2016; 119: 1076-1088. doi: 10. 1161/ CIRCRESAHA. 116. 308895.
42. Fry JL, Shiraishi Y, Turcotte R, Yu X, Gao YZ, Akiki R, Bachschmid M, Zhang Y, Morgan KG, Cohen RA, Seta F. Vascular smooth muscle sirtuin-1 protects against aortic dissection during angiotensin II-induced hypertension. J Am Heart Assoc. 2015; 4: e002384. doi: 10. 1161/ JAHA. 115. 002384.
43. Yoshino J, Mills KF, Yoon MJ, Imai S. Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet-and ageinduced diabetes in mice. Cell Metab. 2011; 14: 528-536. doi: 10. 1016/j. cmet. 2011. 08. 014.
44. Hiratzka LF, Bakris GL, Beckman JA, et al; American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines; American Association for Thoracic Surgery; American College of Radiology; American Stroke Association; Society of Cardiovascular Anesthesiologists; Society for Cardiovascular Angiography and Interventions; Society of Interventional Radiology; Society of Thoracic Surgeons; Society for Vascular Medicine. 2010 ACCF/AHA/ AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the diagnosis and management of patients with Thoracic Aortic Disease: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, American Association for Thoracic Surgery, American College of Radiology, American Stroke Association, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of Thoracic Surgeons, and Society for Vascular Medicine. Circulation. 2010; 121: e266-e369. doi: 10. 1161/CIR. 0b013e3181d4739e.
45. Jiang YZ, Manduchi E, Jiménez JM, Davies PF. Endothelial epigenetics in biomechanical stress: disturbed flow-mediated epigenomic plasticity in vivo and in vitro. Arterioscler Thromb Vasc Biol. 2015; 35: 1317-1326. doi: 10. 1161/ATVBAHA. 115. 303427.