Kleinstiver Lab Publications

​Kleinstiver lab members in bold text.
* co-first author / ^ co-corresponding author

​

Published manuscripts:

​​

1. Mesaki K, Yamamoto H, Juvet S, Yeung J, Guan Z, Akhter A, Yao Y, Dickie C, Mangat H, Wang A, Wilson GW, Mariscal A, Hu J, Davidson AR, Kleinstiver BP, Cypel M, Liu M, Keshavjee S. CRISPR-Cas Genome Editing in Ex Vivo Human Lungs to Rewire the Translational Path of Genome-Targeting Therapeutics. Human Gene Therapy. (2024)

2. McLean ZL, Gao D, Correia K, Roy JCL, Shibata S, Farnum IN, Valdepenas-Mellor Z, Kovalenko M, Rapuru M, Morini E, Ruliera J, Gillis T, Lucente D, Kleinstiver BP, Lee JM, MacDonald ME, Wheeler VC, Mouro Pinto R, Gusella JF. Splice modulators target PMS1 to reduce somatic expansion of the Huntington's disease-associated CAG repeat. Nature Communications. (2024)

3. Fry MY, Navarro PP, Hakim P, Ananda VY, Qin X, Landoni JC, Rath S, Inde Z, Lugo CM, Luce BE, Ge Y, McDonald JL, Ali I, Ha LL, Kleinstiver BP, Chan DC, Sarosiek KA, Chao LH. In situ architecture of Opa1-dependent mitochondrial cristae remodeling. EMBO Journal. (2024)

4. Alves CRR^, Ha LL, Yaworski R, Sutton ER, Lazzarotto CR, Christie KA, Reilly A, Beauvais A, Doll RM, de la Cruz D, Maguire CA, Swoboda KJ, Tsai SQ, Kothary R, Kleinstiver BP. Optimization of base editors for the functional correction of SMN2 as a treatment for spinal muscular atrophy. Nature Biomedical Engineering. (2023)

5. Zhao L, Koseki SRT, Silverstein RA, Amrani N, Peng C, Kramme C, Savic N, Pacesa M, Rodríguez TC, Stan T, Tysinger E, Hong L, Yudistyra V, Ponnapati MR, Jacobson JM, Church GM, Jakimo N, Truant R, Jinek M, Kleinstiver BP, Sontheimer EJ, Chatterjee P. PAM-flexible genome editing with an engineered chimeric Cas9. Nature Communications. (2023)

6. Tao Y, Lamas V, Du W, Zhu W, Li Y, Whittaker MN, Zuris JA, Thompson DB, Rameshbabu AP, Shu Y, Gao X, Hu JH, Pei C, Kong WJ, Liu X, Wu H, Kleinstiver BP, Liu DR, Chen ZY. Treatment of monogenic and digenic dominant genetic hearing loss by CRISPR-Cas9 ribonucleoprotein delivery in vivo. Nature Communications. (2023)

7. Mesaki K, Juvet S, Yeung J, Guan Z, Wilson GW, Hu J, Davidson AR, Kleinstiver BP, Cypel M, Liu M, Keshavjee S. Immunomodulation of the donor lung with CRISPR-mediated activation of IL-10 expression. Journal of Heart and Lung Transplantation. (2023)

8. Peters CW, Hanlon KS, Ivanchenko MV, Zinn E, Linarte EF, Li Y, Levy JM, Liu DR, Kleinstiver BP, Indzhykulian AA, Corey DP. Rescue of hearing by adenine base editing in a humanized mouse model of Usher syndrome type 1F. Molecular Therapy. (2023)

9. Kiss MG, Mindur JE, Yates AG, Lee D, Fullard JF, Anzai A, Poller WC, Christie KA, Iwamoto Y, Roudko V, Downey J, Chan CT, Huynh P, Janssen H, Ntranos A, Hoffmann JD, Jacob W, Goswami S, Singh S, Leppert D, Kuhle J, Kim-Schulze S, Nahrendorf M, Kleinstiver BP, Probert F, Roussos P, Swirski FK, McAlpine CS. Interleukin-3 coordinates glial-peripheral immune crosstalk to incite multiple sclerosis. Immunity. (2023)

10. Wünnemann F, Fotsing Tadjo T, Beaudoin M, Lalonde S, Lo KS, Kleinstiver BP, Lettre G. Multimodal CRISPR perturbations of GWAS loci associated with coronary artery disease in vascular endothelial cells. PLoS Genetics. (2023)

11. Kim YH, Kim N, Okafor I, Choi S, Min S, Lee J, Bae SM, Choi K, Choi J, Harihar V, Kim Y, Kim JS, Kleinstiver BP, Lee JK, Ha T, Kim HH. Sniper2L is a high-fidelity Cas9 variant with high activity. Nature Chemical Biology. (2023)

12. Srivastava S, Shaked HM, Gable K, Gupta SD, Pan X, Somashekarappa N, Han G, Mohassel P, Gotkine M, Doney E, Goldenberg P, Tan QKG, Gong Y, Kleinstiver BP, Wishart B, Cope H, Pires CB, Stutzman HE, Spillmann RC; Undiagnosed Disease Network; Sadjadi R, Elpeleg O, Lee CH, Bellen HJ, Edvardson S, Eichler F, Dunn TM. SPTSSA variants alter sphingolipid synthesis and cause a complex hereditary spastic paraplegia. Brain. (2023)

13. Brault J, Liu T, Liu S, Lawson A, Choi U, Kozhushko N, Bzhilyanskaya V, Pavel-Dinu M, Meis RJ, Eckhaus MA, Burkett SS, Bosticardo M, Kleinstiver BP, Notarangelo LD, Lazzarotto CR, Tsai SQ, Wu X, Dahl GA, Porteus MH, Malech HL, De Ravin SS. CRISPR-Cas9-AAV versus lentivector transduction for genome modification of X-linked severe combined immunodeficiency hematopoietic stem cells. Frontiers in Immunology. (2023)

14. Tou CJ, Orr B, Kleinstiver BP. Precise cut-and-paste DNA insertion using engineered type V-K CRISPR-associated transposases. Nature Biotechnology. (2023)

    • Link to free copy of manuscript​

15. Alonso-Lerma B, Jabalera Y, Samperio S, Morin M, Fernandez A, Hille LT, Silverstein RA, Quesada-Ganuza A, Reifs A, Fernández-Peñalver S, Benitez Y, Soletto L, Gavira JA, Diaz A, Vranken W, Sanchez-Mejias A, Güell M, Mojica FJM, Kleinstiver BP, Moreno-Pelayo MA, Montoliu L, Perez-Jimenez R. Evolution of CRISPR-associated endonucleases as inferred from resurrected proteins. Nature Microbiology. (2023)

16. Kiattisewee C, Karanjia AV, Legut M, Daniloski Z, Koplik SE, Nelson J, Kleinstiver BP, Sanjana NE, Carothers JM, Zalatan JG. Expanding the Scope of Bacterial CRISPR Activation with PAM-Flexible dCas9 Variants. ACS Synthetic Biology. (2022)

17. Christie KA, Guo JA, Silverstein RA, Doll RA, Mabuchi M, Stutzman HE, Lin J, Ma L, Walton RT, Pinello L, Robb GB, Kleinstiver BP. Precise DNA cleavage using CRISPR-SpRYgests. Nature Biotechnology. (2022)

18. Tou CJ, Kleinstiver BP. Recent Advances in Double-Strand Break-Free Kilobase-Scale Genome Editing Technologies. Biochemistry. (2022)

19. Shin JW, Hong EP, Park SS, Choi DE, Seong IS, Whittaker MN, Kleinstiver BP, Chen RZ, Lee JM. Allele-specific silencing of the gain-of-function mutation in Huntington's disease using CRISPR-Cas9. JCI Insight. (2022)

20. Meeske AJ, Johnson MC, Hille LT, Kleinstiver BP, Bondy-Denomy J. Lack of Cas13a inhibition by anti-CRISPR proteins from Leptotrichia prophages. Molecular Cell. (2022)​

21. Vicencio J, Sánchez-Bolaños C, Moreno-Sánchez I, Brena D, Kukhtar D, Ruiz-López M, Cots-Ponjoan M, Vejnar CE, Rubio A, Rodrigo Melero N, Carolis C, Pérez-Pulido AJ, Giráldez AJ, Kleinstiver BP, Cerón J, Moreno-Mateos MA. Genome editing in animals with minimal PAM CRISPR-Cas9 enzymes. Nature Communications. (2022)​​

22. Nieland L, van Solinge TS, Cheah PS, Morsett LM, El Khoury J, Rissman JI, Kleinstiver BP, Broekman MLD, Breakefield XO, Abels ER. CRISPR-Cas knockout of miR21 reduces glioma growth. Molecular Therapy Oncolytics. (2022)

23. Christie KA, Kleinstiver BP. Making the cut with PAMless CRISPR-Cas enzymes. Trends in Genetics. (2021)

24. McAlpine CS, Park J, Griciuc A, Kim E, Choi SH, Iwamoto Y, Kiss MG, Christie KA, Vinegoni C, Poller WC, Mindur JE, Chan CT, He S, Janssen H, Wong LP, Downey J, Singh S, Anzai A, Kahles F, Jorfi M, Feruglio PF, Sadreyev RI, Weissleder R, Kleinstiver BP, Nahrendorf M, Tanzi RE, Swirski FK. Astrocytic interleukin-3 programs microglia and limits Alzheimer's disease. Nature. (2021) 

25. Allouche J, Rachmin I, Adhikari K, Pardo LM, Lee JH, McConnell AM, Kato S, Fan S, Kawakami A, Suita Y, Wakamatsu K, Igras V, Zhang J, Navarro PP, Lugo CM, Noonan HR, Christie KA, Itin K, Mujahid N, Lo JA, Won CH, Evans CL, Weng QY, Wang H, Osseiran S, Lovas A, Németh I, Cozzio A, Navarini AA, Hsiao JJ, Nguyen N, Kemény LV, Iliopoulos O, Berking C, Ruzicka T, Gonzalez-José R, Bortolini MC, Canizales-Quinteros S, Acuna-Alonso V, Gallo C, Poletti G, Bedoya G, Rothhammer F, Ito S, Schiaffino MV, Chao LH, Kleinstiver BP, Tishkoff S, Zon LI, Nijsten T, Ruiz-Linares A, Fisher DE, Roider E. NNT mediates redox-dependent pigmentation via a UVB- and MITF-independent mechanism. Cell. (2021)

26. Hu Y, Stilp AM, McHugh CP, Rao S, Jain D, Zheng X, Lane J, Méric de Bellefon S, Raffield LM, Chen MH, Yanek LR, Wheeler M, Yao Y, Ren C, Broome J, Moon JY, de Vries PS, Hobbs BD, Sun Q, Surendran P, Brody JA, Blackwell TW, Choquet H, Ryan K, Duggirala R, Heard-Costa N, Wang Z, Chami N, Preuss MH, Min N, Ekunwe L, Lange LA, Cushman M, Faraday N, Curran JE, Almasy L, Kundu K, Smith AV, Gabriel S, Rotter JI, Fornage M, Lloyd-Jones DM, Vasan RS, Smith NL, North KE, Boerwinkle E, Becker LC, Lewis JP, Abecasis GR, Hou L, O'Connell JR, Morrison AC, Beaty TH, Kaplan R, Correa A, Blangero J, Jorgenson E, Psaty BM, Kooperberg C, Walton RT, Kleinstiver BP, Tang H, Loos RJF, Soranzo N, Butterworth AS, Nickerson D, Rich SS, Mitchell BD, Johnson AD, Auer PL, Li Y, Mathias RA, Lettre G, Pankratz N, Laurie CC, Laurie CA, Bauer DE, Conomos MP, Reiner AP; NHLBI Trans-Omics for Precision Medicine (TOPMed) Consortium. Whole-genome sequencing association analysis of quantitative red blood cell phenotypes: The NHLBI TOPMed program. American Journal of Human Genetics. (2021)

27. Brault J, Liu TQ, Bello EA, Liu S, Sweeney CL, Meis RJ, Koontz S, Corsino C, Choi U, Vayssière G, Bosticardo M, Dowdell KC, Lazzarotto CR, Clark A, Notarangelo LD, Ravell JC, Lenardo MJ, Kleinstiver BP, Tsai S, Wu X, Dahl GA, Malech HL, De Ravin SS. CRISPR-targeted MAGT1 insertion restores XMEN patient hematopoietic stem cells and lymphocytes. Blood. (2021)

28. De Ravin SS, Brault J, Meis RJ, Liu S, Li L, Pavel-Dinu M, Lazzarotto CR, Liu T, Koontz SM, Choi U, Sweeney CL, Theobald N, Lee G, Clark AB, Burkett SS, Kleinstiver BP, Porteus MH, Tsai S, Kuhns DB, Dahl GA, Headey S, Wu X, Malech HL. Enhanced homology-directed repair for highly efficient gene editing in hematopoietic stem/progenitor cells. Blood. (2021)

29. Walton RT, Hsu JY, Joung JK, Kleinstiver BP. Scalable characterization of the PAM requirements of CRISPR-Cas enzymes using HT-PAMDA. Nature Protocols. (2021)

30. Hille LT, Kleinstiver BP. Plant genome editing branches out. Nature Plants. (2021) 

31. Neggers JE, Jacquemyn M, Dierckx T, Kleinstiver BP, Thibaut HJ, Daelemans D. enAsCas12a Enables CRISPR-Directed Evolution to Screen for Functional Drug Resistance Mutations in Sequences Inaccessible to SpCas9. Molecular Therapy (2021)

32. DeWeirdt PC, Sanson KR, Sangree AK, Hegde M, Hanna RE, Feeley MN, Griffith AL, Teng T, Borys SM, Strand C, Joung JK, Kleinstiver BP, Pan X, Huang A, Doench JG. Optimization of AsCas12a for combinatorial genetic screens in human cells. Nature Biotechnology. (2021) 

33. Schmidts A, Marsh LC, Srivastava AA, Bouffard AA, Boroughs AC, Scarfò I, Larson RC, Bedoya F, Choi BD, Frigault MJ, Bailey SR, Leick MB, Vatsa S, Kann MC, Prew MS, Kleinstiver BP, Joung JK, Maus MV. Cell-based artificial APC resistant to lentiviral transduction for efficient generation of CAR-T cells from various cell sources. Journal for ImmunoTherapy of Cancer. (2020)

34. Cruz L, György B, Cheah PS, Kleinstiver BP, Eimer WA, Garcia SP, Sharma N, Ozelius LJ, Bragg DC, Joung JK, Norberto de Souza O, Macedo Timmers LFS, Breakefield XO. Mutant Allele-Specific CRISPR Disruption in DYT1 Dystonia Fibroblasts Restores Cell Function. Molecular Therapy Nucleic Acids. (2020)

35. Osuna BA, Karambelkar S, Mahendra C, Christie KA, Garcia B, Davidson AR, Kleinstiver BP, Kilcher S, Bondy-Denomy J. Listeria Phages Induce Cas9 Degradation to Protect Lysogenic Genomes. Cell Host Microbe. (2020)

36. Mahendra C, Christie KA, Osuna BA, Pinilla-Redondo R, Kleinstiver BP, Bondy-Denomy J. Broad-spectrum anti-CRISPR proteins facilitate horizontal gene transfer. Nature Microbiology. (2020)

37. Walton RT, Christie KA, Whittaker MN, Kleinstiver BP. Unconstrained genome targeting with near-PAMless engineered CRISPR-Cas9 variants. Science. (2020)

38. Breuer CB, Hanlon KS, Natasan JS, Volak A, Meliani A, Mingozzi F, Kleinstiver BP, Moon JJ, Maguire CA. In vivo engineering of lymphocytes after systemic exosome-associated AAV delivery. Scientific Reports. (2020)

39. Hanlon KS, Kleinstiver BP, Garcia SP, Zaborowski MP, Volak A, Spirig SE, Muller A, Sousa AA, Tsai SQ, Bengtsson NE, Lööv C, Ingelsson M, Chamberlain JS, Corey DP, Aryee MJ, Joung JK, Breakefield XO, Maguire CA, György B. High levels of AAV vector integration into CRISPR-induced DNA breaks. Nature Communications. (2019)

40. Anikeeva P, Boyden E, Brangwynne C, Cissé II, Fiehn O, Fromme P, Gingras AC, Greene CS, Heard E, Hell SW, Hillman E, Jensen GJ, Karchin R, Kiessling LL, Kleinstiver BP, Knight R, Kukura P, Lancaster MA, Loman N, Looger L, Lundberg E, Luo Q, Miyawaki A, Myers EW Jr, Nolan GP, Picotti P, Reik W, Sauer M, Shalek AK, Shendure J, Slavov N, Tanay A, Troyanskaya O, van Valen D, Wang HW, Yi C, Yin P, Zernicka-Goetz M, Zhuang X. Voices in methods development. Nature Methods. (2019)

41. György B, Nist-Lund C, Pan B, Asai Y, Karavitaki KD, Kleinstiver BP, Garcia SP, Zaborowski MP, Solanes P, Spataro S, Schneider BL, Joung JK, Géléoc GSG, Holt JR, Corey DP. Allele-specific gene editing prevents deafness in a model of dominant progressive hearing loss. Nature Medicine. (2019)

42. Kleinstiver BP^, Sousa AA, Walton RT, Tak YE, Hsu JY, Clement K, Welch MM, Horng JE, Malagon-Lopez J, Scarfò I, Maus MV, Pinello L, Aryee MJ, Joung JK. Engineered CRISPR-Cas12a variants with increased activities and improved targeting ranges for gene, epigenetic and base editing. Nature Biotechnology. (2019)

43. Lee K, Zhang Y, Kleinstiver BP, Guo JA, Aryee MJ, Miller J, Malzahn A, Zarecor S, Lawrence-Dill CJ, Joung JK, Qi Y, Wang K. Activities and specificities of CRISPR/Cas9 and Cas12a nucleases for targeted mutagenesis in maize. Plant Biotechnology Journal. (2019)

44. Marino ND, Zhang JY, Borges AL, Sousa AA, Leon LM, Rauch BJ, Walton RT, Berry JD, Joung JK, Kleinstiver BP, Bondy-Denomy J. Discovery of widespread type I and type V CRISPR-Cas inhibitors. Science. (2018)

45. Listgarten J, Weinstein M, Kleinstiver BP, Sousa AA, Joung JK, Crawford J, Gao K, Hoang L, Elibol M, Doench JG, Fusi N. Prediction of off-target activities for the end-to-end design of CRISPR guide RNAs. Nature Biomedical Engineering. (2018)

46. György B, Lööv C, Zaborowski MP, Takeda S, Kleinstiver BP, Commins C, Kastanenka K, Mu D, Volak A, Giedraitis V, Lannfelt L, Maguire CA, Joung JK, Hyman BT, Breakefield XO, Ingelsson M. CRISPR/Cas9 Mediated Disruption of the Swedish APP Allele as a Therapeutic Approach for Early-Onset Alzheimer's Disease. Molecular Therapy Nucleic Acids. (2018)

47. Chowdhury TA, Koceja C, Eisa-Beygi S, Kleinstiver BP, Kumar SN, Lin CW, Li K, Prabhudesai S, Joung JK, Ramchandran R. Temporal and Spatial Post-Transcriptional Regulation of Zebrafish tie1 mRNA by Long Noncoding RNA During Brain Vascular Assembly. Arteriosclerosis, Thrombosis, and Vascular Biology. (2018)

48. Li P, Kleinstiver BP, Leon MY, Prew MS, Navarro-Gomez D, Greenwald SH, Pierce EA, Joung JK, Liu Q. Allele-Specific CRISPR-Cas9 Genome Editing of the Single-Base P23H Mutation for Rhodopsin-Associated Dominant Retinitis Pigmentosa. The CRISPR Journal (2018)

49. Ando K, Shah AK, Sachdev V, Kleinstiver BP, Taylor-Parker J, Welch MM, Hu Y, Salgia R, White FM, Parvin JD, Ozonoff A, Rameh LE, Joung JK, Bharti AK. Camptothecin resistance is determined by the regulation of topoisomerase I degradation mediated by ubiquitin proteasome pathway. Oncotarget. (2017)

50. Tak YE, Kleinstiver BP, Nuñez JK, Hsu JY, Horng JE, Gong J, Weissman JS, Joung JK. Inducible and multiplex gene regulation using CRISPR-Cpf1-based transcription factors. Nature Methods. (2017)

51. Chen JS*, Dagdas YS*, Kleinstiver BP*, Welch MM, Sousa AA, Harrington LB, Sternberg SH, Joung JK, Yildiz A, Doudna JA. Enhanced proofreading governs CRISPR-Cas9 targeting accuracy. Nature. (2017

52. Kleinstiver BP*^, Tsai SQ*, Prew MS, Nguyen NT, Welch MM, Lopez JM, McCaw ZR, Aryee MJ, Joung JK. Genome-wide specificities of CRISPR-Cas Cpf1 nucleases in human cells. Nature Biotechnology. (2016)

53. Saha SK, Gordan JD, Kleinstiver BP, Vu P, Najem MS, Yeo JC, Shi L, Kato Y, Levin RS, Webber JT, Damon LJ, Egan RK, Greninger P, McDermott U, Garnett MJ, Jenkins RL, Rieger-Christ KM, Sullivan TB, Hezel AF, Liss AS, Mizukami Y, Goyal L, Ferrone CR, Zhu AX, Joung JK, Shokat KM, Benes CH, Bardeesy N. Isocitrate Dehydrogenase Mutations Confer Dasatinib Hypersensitivity and SRC Dependence in Intrahepatic Cholangiocarcinoma. Cancer Discovery. (2016)

54. Kleinstiver BP*, Pattanayak V*, Prew MS, Tsai SQ, Nguyen NT, Zheng Z, Joung JK. High-fidelity CRISPR-Cas9 nucleases with no detectable genome-wide off-target effects. Nature. (2016) 

55. Kleinstiver BP^, Prew MS, Tsai SQ, Nguyen NT, Topkar VV, Zheng Z, Joung JK. Broadening the targeting range of Staphylococcus aureus CRISPR-Cas9 by modifying PAM recognition. Nature Biotechnology. (2015)

56. Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, Gonzales AP, Li Z, Peterson RT, Yeh JR, Aryee MJ, Joung JK. Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature. (2015)

57. Black JC, Atabakhsh E, Kim J, Biette KM, Van Rechem C, Ladd B, Burrowes PD, Donado C, Mattoo H, Kleinstiver BP, Song B, Andriani G, Joung JK, Iliopoulos O, Montagna C, Pillai S, Getz G, Whetstine JR. Hypoxia drives transient site- specific copy gain and drug-resistant gene expression. Genes and Development. (2015)

58. Kleinstiver BP*, Wang L*, Wolfs JM, Kolaczyk T, McDowell B, Wang X, Schild-Poulter C, Bogdanove AJ, Edgell DR. The I-TevI nuclease and linker domains contribute to the specificity of monomeric TALENs. G3. (2014)

59. Wolfs JM, Kleinstiver BP, Edgell DR. Rapid screening of endonuclease target site preference using a modified bacterial two-plasmid selection. Methods of Molecular Biology. (2014)

60. Kleinstiver BP, Wolfs JM, Edgell DR. The monomeric GIY-YIG homing endonuclease I-BmoI uses a molecular anchor and a flexible tether to sequentially nick DNA. Nucleic Acids Research. (2013) 

61. Kleinstiver BP, Wolfs JM, Kolaczyk T, Roberts AK, Hu SX, Edgell DR. Monomeric site-specific nucleases for genome editing. Proceedings of the National Academy of Science USA. (2012)

62. Kleinstiver BP, Bérubé-Janzen W, Fernandes AD, Edgell DR. Divalent metal ion differentially regulates the sequential nicking reactions of the GIY-YIG homing endonuclease I-BmoI. PLoS One. (2011)

63. Fernandes AD, Kleinstiver BP, Edgell DR, Wahl LM, Gloor GB. Estimating the evidence of selection and the reliability of inference in unigenic evolution. Algorithms of Molecular Biology. (2010) 

64. Kleinstiver BP, Fernandes AD, Gloor GB, Edgell DR. A unified genetic, computational and experimental framework identifies functionally relevant residues of the homing endonuclease I-BmoI. Nucleic Acids Research. (2010)

65. Carter JM, Friedrich NC, Kleinstiver B, Edgell DR. Strand-specific contacts and divalent metal ion regulate double-strand break formation by the GIY-YIG homing endonuclease I-BmoI. Journal of Molecular Biology. (2007)