CRISPR engineering cardiometabolic disease models using human iPSC

Cindy E. McKinney; Katherine M. Baumgarner

doi:10.3934/celltissue.2018.3.185

AIMS Cell and Tissue Engineering, 2018, 2(3): 185-202. doi: 10.3934/celltissue.2018.3.185. Review Special Issues

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CRISPR engineering cardiometabolic disease models using human iPSC

Cindy E. McKinney, Katherine M. Baumgarner

iPSC and Stem Cell Lab, Edward Via College of Osteopathic Medicine and Gibbs Research Institute, Spartanburg, SC 29303

Received: , Accepted: , Published:

Special Issues: iPS Cell Technologies in Human Diseases

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Since their introduction, human induced pluripotent stem cells (iPSCs) have enhanced the ways human disease processes are evaluated. Only eleven years ago, Yamanaka and colleagues showed somatic cells could be reprogrammed to induced pluripotent cells (iPSC) employing four transcription factors. Since that initial demonstration, much progress has been made in establishing human cardiac cell models that recapitulate diseases using easily obtained patient somatic cells such as fibroblasts or peripheral blood cells. Investigators now have access, through established small molecule methods to differentiate iPSCs to cardiomyocytes, hepatocytes, neurons, astrocytes and many other cell types of interest. This capability provides valuable cell models of human disease derived from patient cells or CRISPR gene-edited cells that introduce or repair patient disease mutations. In many cases, these manipulations create unique cell models and address the need for scalability and reproducibility of cell samples. Consequently, human iPSC derived cells can be used to query cellular and pathological mechanisms potentially providing bio-information that animal models may be unable to report. In this article, we review iPSC derived cardiomyocyte models of cardiometabolic disease and demonstrate the power of these technologies to probe gene function for biological and clinical significance and to capture pathological signatures from genetic variation in human cardiac disease. Examples of the iPSC derived cardiometabolic disease models including channelopathies, metabolic disease and cardiomyopathy are presented.

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Keywords: iPSC; cardiomyocytes; CRISPR/Cas9 editing; cardiomyopathies; disease models

Citation: Cindy E. McKinney, Katherine M. Baumgarner. CRISPR engineering cardiometabolic disease models using human iPSC. AIMS Cell and Tissue Engineering, 2018, 2(3): 185-202. doi: 10.3934/celltissue.2018.3.185

References:

1. Orban JC, Walrave Y, Mongardon N, et al. (2017) Causes and characteristics of death in intensive care units. Anesthesiology 126: 882–889.
2. Lovett M, Lee K, Edwards A, et al. (2009) Vascularization strategies for tissue engineering. Tissue Eng Part B Rev 15: 353–370.
3. Griffith CK, Miller C, Sainson RCA, et al. (2005) Diffusion limits of an in vitro thick prevascularized tissue. Tissue Eng 11: 257–266.
4. Jain RK, Au P, Tam J, et al. (2005) Engineering vascularized tissue. Nat Biotechnol 23: 821–823.
5. Phelps EA, García AJ (2010) Engineering more than a cell: Vascularization strategies in tissue engineering. Curr Opin Biotechnol 21: 704–709.
6. Bertassoni LE, Cecconi M, Manoharan V, et al. (2014) Hydrogel bioprinted microchannel networks for vascularization of tissue engineering constructs. Lab Chip 14: 2202–2211.
7. Rouwkema J, Rivron NC, van Blitterswijk CA (2008) Vascularization in tissue engineering. Trends Biotechnol 26: 434–441.
8. Ikada Y (2006) Challenges in tissue engineering. J R Soc Interface 3: 589–601.
9. Griffith LG, Naughton G (2002) Tissue engineering--current challenges and expanding opportunities. Science 295: 1009–1014.
10. Kang HW, Lee SJ, Ko IK, et al. (2016) A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol 34: 312–319.
11. Berthiaume F, Maguire TJ, Yarmush ML (2011) CH02CH19-Yarmush. Annu Rev Chem Biomol Eng 2: 403–430.
12. Hollister SJ (2005) Porous scaffold design for tissue engineering. Nat Mater 4: 518–524.
13. Chan BP, Leong KW (2008) Scaffolding in tissue engineering: general approaches and tissue-specific considerations. Eur Spine J 17: 467–479.
14. Novosel EC, Kleinhans C, Kluger PJ (2011) Vascularization is the key challenge in tissue engineering. Adv Drug Deliv Rev 63: 300–311.
15. Zhao X, Liu L, Wang J, et al. (2016) In vitro vascularization of a combined system based on a 3D printing technique. J Tissue Eng Regen Med 10: 833–842.
16. Pashneh-Tala S, MacNeil S, Claeyssens F (2015) The tissue-engineered vascular graft-past, present, and future. Tissue Eng Part B Rev 22.
17. O'Brien FJ (2011) Biomaterials & scaffolds for tissue engineering. Mater Today 14: 88–95.
18. He Y, Lu F (2016) Development of synthetic and natural materials for tissue engineering applications using adipose stem cells. Stem Cells Int 2016: 5786257.
19. Kim JJ, Hou L, Yang G, et al. (2017) Microfibrous scaffolds enhance endothelial differentiation and organization of induced pluripotent stem cells. Cell Mol Bioeng 10: 417–432.
20. Plunkett N, O'Brien FJ (2010) IV.3. Bioreactors in tissue engineering. Stud Health Technol Inform 152: 214–230.
21. Kolesky DB, Homan KA, Skylar-Scott MA, et al. (2016) Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci 113: 3179–3184.
22. Kolte D, McClung JA, Aronow WS (2016) Vasculogenesis and angiogenesis. Transl Res in Coron Artery Dis 49–65.
23. Risau W (1997) Mechanisms of angiogenesis. Nat 386: 671–674.
24. Carmeliet P, Jain RK (2000) Angiogenesis in cancer and other diseases. Nat 407: 249–257.
25. Carmeliet P (2000) Mechanisms of angiogenesis and arteriogenesis. Nat Med 6: 389–395.
26. Lanza RP, Langer RS, Vacanti J (2014) Principles of Tissue Engineering. Elsevier.
27. Gao Y (2017) Biology of Vascular Smooth Muscle: Vasoconstriction and Dilatation, Singapore: Springer Singapore.
28. Ardalani H, Assadi AH, Murphy WL (2014) Structure, function, and development of blood vessels: lessons for tissue engineering. In, Engineering in Translational Medicine, London: Springer London, 155–182.
29. Rhodin JAG (1980) Architecture of the vessel wall. In, Comprehensive Physiology, Hoboken: John Wiley & Sons, 1–31.
30. Kossmann CE, Palade GE (1961) Blood capillaries of the heart and other organs. Circulation 24: 368–384.
31. Burton AC (1954) Relation of structure to function of the tissues of the wall of blood vessels. Physiol Rev 34: 619–642.
32. Yamamoto H, Ehling M, Kato K, et al. (2015) Integrin β1 controls VE-cadherin localization and blood vessel stability. Nat Commun 6: 6429.
33. Okabe E, Todoki K, Ito H (1990) Microcirculation: function and regulation in microvasculature. In, Dynamic Aspects of Dental Pulp, Dordrecht: Springer Netherlands, pp 151–166.
34. Ji S, Guvendiren M (2017) Recent advances in bioink design for 3D bioprinting of tissues and organs. Front Bioeng Biotechnol 5: 23.
35. Hölzl K, Lin S, Tytgat L, et al. (2016) Bioink properties before, during and after 3D bioprinting. Biofabrication 8: 032002.
36. Hospodiuk M, Dey M, Sosnoski D, et al. (2017) The bioink: A comprehensive review on bioprintable materials. Biotechnol Adv 35: 217–239.
37. Smith CM, Stone AL, Parkhill RL, et al. (2004) Three-dimensional bioassembly tool for generating viable tissue-engineered constructs. Tissue Eng 10: 1566–1576.
38. Chen CY, Barron JA, Ringeisen BR (2006) Cell patterning without chemical surface modification: cell–cell interactions between printed bovine aortic endothelial cells (BAEC) on a homogeneous cell-adherent hydrogel. Appl Surf Sci 252: 8641–8645.
39. Gao Q, He Y, Fu J, et al. (2015) Coaxial nozzle-assisted 3D bioprinting with built-in microchannels for nutrients delivery. Biomater 61: 203–215.
40. Norotte C, Marga FS, Niklason LE, et al. (2009) Scaffold-free vascular tissue engineering using bioprinting. Biomaterials 30: 5910–5917.
41. Zhang YS, Arneri A, Bersini S, et al. (2016) Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomater 110: 45–59.
42. Lee VK, Kim DY, Ngo H, et al. (2014) Creating perfused functional vascular channels using 3D bio-printing technology. Biomater 35: 8092–8102.
43. Yin Yu, Ozbolat IT (2014) Tissue strands as "bioink" for scale-up organ printing. Conf Proc IEEE Eng Med Biol Soc 2014: 1428–1431.
44. Wilkens CA, Rivet CJ, Akentjew TL, et al. (2016) Layer-by-layer approach for a uniformed fabrication of a cell patterned vessel-like construct. Biofabrication 9: 015001.
45. Cui X, Boland T (2009) Human microvasculature fabrication using thermal inkjet printing technology. Biomater 30: 6221–6227.
46. Darland DC, Massingham LJ, Smith SR, et al. (2003) Pericyte production of cell-associated VEGF is differentiation-dependent and is associated with endothelial survival. Dev Biol 264: 275–288.
47. Korff T, Kimmina S, Martiny-Baron G, et al. (2001) Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J 15: 447–457.
48. Lee VK, Lanzi AM, Ngo H, et al. (2014) Generation of Multi-scale Vascular Network System Within 3D Hydrogel Using 3D Bio-printing Technology. Cell Mol Bioeng 7: 460–472.
49. Jia W, Gungor-Ozkerim PS, Zhang YS, et al. (2016) Direct 3D bioprinting of perfusable vascular constructs using a blend bioink. Biomater 106: 58–68.
50. Jang J, Park HJ, Kim SW, et al. (2017) 3D printed complex tissue construct using stem cell-laden decellularized extracellular matrix bioinks for cardiac repair. Biomater 112: 264–274.
51. Jia J, Richards DJ, Pollard S, et al. (2014) Engineering alginate as bioink for bioprinting. Acta Biomater 10: 4323–4331.
52. Das S, Pati F, Choi YJ, et al. (2015) Bioprintable, cell-laden silk fibroin–gelatin hydrogel supporting multilineage differentiation of stem cells for fabrication of three-dimensional tissue constructs. Acta Biomater 11: 233–246.
53. Blaeser A, Duarte Campos DF, Puster U, et al. (2016) Controlling shear stress in 3D bioprinting is a key factor to balance printing resolution and stem cell integrity. Adv Healthc Mater 5: 326–333.
54. Hipp J, Atala A (2008) Sources of stem cells for regenerative medicine. Stem Cell Rev 4: 3–11.
55. Wilson KD, Wu JC (2015) Induced pluripotent stem cells. JAMA 313: 1613.
56. Wong CW, Chen YT, Chien CL, et al. (2018) A simple and efficient feeder-free culture system to up-scale iPSCs on polymeric material surface for use in 3D bioprinting. Mater Sci Eng C 82: 69–79.
57. Faulkner-Jones A, Fyfe C, Cornelissen DJ, et al. (2015) Bioprinting of human pluripotent stem cells and their directed differentiation into hepatocyte-like cells for the generation of mini-livers in 3D. Biofabrication 7: 044102.
58. Ma X, Qu X, Zhu W, et al. (2016) Deterministically patterned biomimetic human iPSC-derived hepatic model via rapid 3D bioprinting. Proc Natl Acad Sci 113: 2206–2211.
59. Miller JS, Stevens KR, Yang MT, et al. (2012) Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater 11: 768–774.
60. Kolesky DB, Truby RL, Gladman AS, et al. (2014) 3D bioprinting of vascularized, heterogeneous cell-laden tissue constructs. Adv Mater 26: 3124–3130.
61. Sukmana I (2012) Microvascular guidance: a challenge to support the development of vascularised tissue engineering construct. The Sci World J 2012: 201352.
62. Kim JA, Kim HN, Im SK, et al. (2015) Collagen-based brain microvasculature model in vitro using three-dimensional printed template. Biomicrofluidics 9: 024115.
63. Muscari C, Giordano E, Bonafè F, et al. (2014) Strategies affording prevascularized cell-based constructs for myocardial tissue engineering. Stem Cells Int 2014: 434169.
64. Bogorad MI, DeStefano J, Karlsson J, et al. (2015) Review: in vitro microvessel models. Lab Chip 15: 4242–4255.
65. Moon JJ, West JL (2008) Vascularization of engineered tissues: approaches to promote angio-genesis in biomaterials. Curr Top Med Chem 8: 300–310.
66. Yang P, Huang X, Shen J, et al. (2013) Development of a new pre-vascularized tissue-engineered construct using pre-differentiated rADSCs, arteriovenous vascular bundle and porous nano-hydroxyapatide-polyamide 66 scaffold. BMC Musculoskelet Disord 14: 318.
67. Zhu W, Qu X, Zhu J, et al. (2017) Direct 3D bioprinting of prevascularized tissue constructs with complex microarchitecture. Biomater 124: 106–115.
68. Mirabella T, MacArthur JW, Cheng D, et al. (2017) 3D-printed vascular networks direct therapeutic angiogenesis in ischaemia. Nat Biomed Eng 1: 0083.
69. Gelber MK, Hurst G, Comi TJ, et al. (2018) Model-guided design and characterization of a high-precision 3D printing process for carbohydrate glass. Addit Manuf 22: 38–50.
70. Xu C, Lee W, Dai G, et al. (2018) Highly elastic biodegradable single-network hydrogel for cell printing. ACS Appl Mater Interfaces 10: 9969–9979.
71. Hinton TJ, Jallerat Q, Palchesko RN, et al. (2015) Three-dimensional printing of complex biological structures by freeform reversible embedding of suspended hydrogels. Sci Adv 1: e1500758–e1500758.
72. Suntornnond R, Tan EYS, An J, et al. (2017) A highly printable and biocompatible hydrogel composite for direct printing of soft and perfusable vasculature-like structures. Sci Rep 7: 1–11.
73. Lee V, Singh G, Trasatti JP, et al. (2014) Design and Fabrication of Human Skin by Three-Dimensional Bioprinting. Tissue Eng Part C Methods 20: 473–484.
74. Qilong Z, Juan W, Huanqing C, et al. (2018) Programmed shape‐morphing scaffolds enabling facile 3D endothelialization. Adv Funct Mater 0: 1801027.
75. Yu Y, Moncal KK, Li J, et al. (2016) Three-dimensional bioprinting using self-assembling scalable scaffold-free "tissue strands" as a new bioink. Sci Rep 6: 28714.
76. Xu C, Chai W, Huang Y, et al. (2012) Scaffold-free inkjet printing of three-dimensional zigzag cellular tubes. Biotechnol Bioeng 109: 3152–3160.
77. Zhang Y, Yu Y, Chen H, et al. (2013) Characterization of printable cellular micro-fluidic channels for tissue engineering. Biofabrication 5: 25004.
78. Visser CW, Kamperman T, Karbaat LP, et al. (2018) In-air microfluidics enables rapid fabrication of emulsions, suspensions, and 3D modular (bio)materials. Sci Adv 4: 1–9.
79. Daniel JT, Jessop ZM, Whitaker IS (2017) 3D Bioprinting for Reconstructive Surgery Techniques and Applications. Woodhead Publishing.
80. Mandrycky C, Wang Z, Kim K, et al. (2016) 3D bioprinting for engineering complex tissues. Biotechnol Adv 34: 422–434.
81. Catros S, Fricain JC, Guillotin B, et al. (2011) Laser-assisted bioprinting for creating on-demand patterns of human osteoprogenitor cells and nano-hydroxyapatite. Biofabrication 3: 025001.
82. Catros S, Guillotin B, Bačáková M, et al. (2011) Effect of laser energy, substrate film thickness and bioink viscosity on viability of endothelial cells printed by laser-assisted bioprinting. Appl Surf Sci 257: 5142–5147.
83. Grogan SP, Chung PH, Soman P, et al. (2013) Digital micromirror device projection printing system for meniscus tissue engineering. Acta Biomater 9: 7218–7226.
84. Sorkio A, Koch L, Koivusalo L, et al. (2018) Human stem cell based corneal tissue mimicking structures using laser-assisted 3D bioprinting and functional bioinks. Biomater 171: 57–71.
85. Gruene M, Pflaum M, Deiwick A, et al. (2011) Adipogenic differentiation of laser-printed 3D tissue grafts consisting of human adipose-derived stem cells. Biofabrication 3: 015005.
86. Foyt DA, Norman MDA, Yu TTL, et al. (2018) Exploiting advanced hydrogel technologies to address key challenges in regenerative medicine. Adv Healthc Mater 7: 1700939.
87. Shanjani Y, Pan CC, Elomaa L, et al. (2015) A novel bioprinting method and system for forming hybrid tissue engineering constructs. Biofabrication 7: 045008.
88. Aguilar JP, Lipka M, Primo GA, et al. (2018) 3D Electrophoresis-assisted lithography (3DEAL): 3D molecular printing to create functional patterns and anisotropic hydrogels. Adv Funct Mater 28: 1–10.
89. Hribar KC, Meggs K, Liu J, et al. (2015) Three-dimensional direct cell patterning in collagen hydrogels with near-infrared femtosecond laser. Sci Rep 5: 17203.
90. Wang Z, Jin X, Dai R, et al. (2016) An ultrafast hydrogel photocrosslinking method for direct laser bioprinting. RSC Adv 6: 21099–21104.
91. Miri AK, Nieto D, Iglesias L, et al. (2018) Microfluidics-enabled multimaterial maskless stereolithographic bioprinting. Adv Mater 30: e1800242.
92. Mosadegh B, Xiong G, Dunham S, et al. (2015) Current progress in 3D printing for cardiovascular tissue engineering. Biomed Mater 10: 034002.
93. Ringeisen BR, Pirlo RK, Wu PK, et al. (2013) Cell and organ printing turns 15: Diverse research to commercial transitions. MRS Bull 38: 834–843.
94. Duan B (2017) State-of-the-art review of 3D bioprinting for cardiovascular tissue engineering. Ann Biomed Eng 45: 195–209.
95. Gao Q, Liu Z, Lin Z, et al. (2017) 3D bioprinting of vessel-like structures with multilevel fluidic channels. ACS Biomater Sci Eng 3: 399–408.
96. Khademhosseini A, Camci-Unal G (2018) 3D Bioprinting in Regenerative Engineering: Principles and Applications. CRC Press.
97. Wu Y, Lin ZY (William), Wenger AC, et al. (2018) 3D bioprinting of liver-mimetic construct with alginate/cellulose nanocrystal hybrid bioink. Bioprinting 9: 1–6.
98. Visconti RP, Kasyanov V, Gentile C, et al. (2010) Towards organ printing: engineering an intra-organ branched vascular tree. Expert Opin Biol Ther 10: 409–420.
99. Prendergast ME, Montoya G, Pereira T, et al. (2018) Microphysiological systems: automated fabrication via extrusion bioprinting. Microphysiological Syst 2: 1–16.
100. Charbe N, McCarron PA, Tambuwala MM (2017) Three-dimensional bio-printing: A new frontier in oncology research. World J Clin Oncol 8: 21–36.
101. Gopinathan J, Noh I (2018) Recent trends in bioinks for 3D printing. Biomater Res 22: 11.
102. Guvendiren M, Molde J, Soares RMD, et al. (2016) Designing biomaterials for 3d printing. ACS Biomater Sci Eng 2: 1679–1693.
103. Gu Q, Tomaskovic-Crook E, Wallace GG, et al. (2017) 3D bioprinting human induced pluripotent stem cell constructs for in situ cell proliferation and successive multilineage differentiation. Adv Healthc Mater 6: 1700175.
104. Ong CS, Fukunishi T, Zhang H, et al. (2017) Biomaterial-free three-dimensional bioprinting of cardiac tissue using human induced pluripotent stem cell derived cardiomyocytes. Sci Rep 7: 4566.
105. Medvedev SP, Shevchenko AI, Zakian SM (2010) Induced pluripotent stem cells: problems and advantages when applying them in regenerative medicine. Acta Nat 2: 18–28.
106. Wang W, Yang J, Liu H, et al. (2011) Rapid and efficient reprogramming of somatic cells to induced pluripotent stem cells by retinoic acid receptor gamma and liver receptor homolog 1. Proc Natl Acad Sci 108: 18283–18288.
107. Tidball AM, Dang LT, Glenn TW, et al. (2017) Rapid generation of human genetic loss-of-function ipsc lines by simultaneous reprogramming and gene editing. Stem Cell Reports 9: 725–731.
108. Rutz AL, Hyland KE, Jakus AE, et al. (2015) A multi-material bioink method for 3D printing tunable, cell-compatible hydrogels. Adv Mater 27: 1607–1614.
109. Vatani M, Choi JW (2017) Direct-print photopolymerization for 3D printing. Rapid Prototyp J 23: 337–343.
110. Tappa K, Jammalamadaka U (2018) Novel biomaterials used in medical 3D printing techniques. J Funct Biomater 9: 17.
111. Aljohani W, Ullah MW, Zhang X, et al. (2018) Bioprinting and its applications in tissue engineering and regenerative medicine. Int J Biol Macromol 107: 261–275.

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