Division of Gastroenterology & Liver Diseases

Erik L. Snapp, Ph.D.

Dr. Erik L. Snapp

Professional Interests

Our lab studies the quality control machinery of the endoplasmic reticulum (ER) in health and disease. In particular, we are interested in how stress changes the organization and function of ER chaperones in diseases ranging from a1-antitrypsin deficiency to chemical stresses. We use a combination of live cell microscopy, development of fluorescent biosensors, and standard biochemistry to understand the cell biology of the Unfolded Protein Response (UPR) and novel quality control pathways.  Current projects include:

- Organization and dynamics of ER chaperones in living cells

- Improvement of fluorescent proteins and biosensors for oxidizing environments

- Quality Control steps for misfolded secretory proteins beyond the endoplasmic reticulum


Selected Publications

Journal Articles and Reviews

1. Snapp EL and Landfear SM. 1997. Cytoskeletal association is important for differential targeting of glucose transporter isoforms in Leishmania enriettii. J Cell Biol. 139:1775-1783. PMCID: PMC2132635

2. Snapp EL and Landfear SM. 1999. Characterization of a targeting motif for a flagellar membrane protein in Leishmania enriettii. J Biol Chem. 274: 29543-29548. no PMCID.

3. Nehls S, Snapp EL, Cole NB, Zaal KJM, Kenworthy AK, Roberts TH, Ellenberg J, Presley JF, Siggia E, and Lippincott-Schwartz J. 2000.Dynamics and retention of misfolded proteins in native ER membranes. Nat Cell Biol. 2:288-295. no PMCID.

4. Lippincott-Schwartz J, Snapp E, and Kenworthy A. 2001. Studying protein dynamics in living cells. Nat Rev Mol Cell Biol. 2:444-456. no PMCID.

5. Brandizzi F, Snapp EL, Roberts A, Lippincott-Schwartz J, and Hawes C. 2002. Membrane protein transport between the endoplasmic reticulum and the Golgi in tobacco leaves is energy dependent but cytoskeleton independent: evidence from selective photobleaching. Plant Cell. 14:1293-1309. PMCID: PMC150781.

6. Nikonov A, Snapp E, Lippincott-Schwartz J, and Kreibich G. 2002. Active translocon complexes labeled with GFP-Dad1 diffuse slowly as large polysome arrays in the endoplasmic reticulum. J Cell Biol. 158:497-506. PMCID: PMC2173836.

7. Snapp EL, Hegde R, Francolini M, Lombardo F, Colombo S, Pedrazzini E, Borgese N, and Lippincott-Schwartz J. 2003. Formation of stacked cisternae by low affinity protein interactions. J Cell Biol. 163:257-269. PMCID: PMC2173526.

8. Snapp EL, Reinhart G, Bogert B, Lippincott-Schwartz J, and Hegde R. 2004. The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells. J Cell Biol. 164:997-1007. PMCID: PMC2172055.

9. daSilva LLP, Snapp EL, Denecke J, Lippincott-Schwartz J, Hawes C, and Brandizzi F. 2004. ER exit sites and Golgi bodies in plant cells form mobile, secretory units. Plant Cell. 16:1753-1771. PMCID: PMC514159.

10. Snapp EL, Iida, T., Frescas, D., Lippincott-Schwartz, J., and Lilly, M. 2004. The fusome mediates intercellular ER connectivity in Drosophila ovarian cysts. Mol Biol Cell. 15:4512-4521. PMCID: PMC519145.

11. Shen J, Snapp E, Lippincott-Schwartz J, and Prywes R. 2005. ER stress causes specific dissociation of a stable ATF-6-BIP complex. Mol Cell Biol. 25:921-932. PMCID: PMC543992.

12. Fontanini A, Chies R, Snapp EL, Ferrarini M, Fabrizi G, and Brancolini C. 2005. Glycan-independent role of calnexin in the intracellular retention of Charcot-Marie-Tooth 1A Gas3/PMP22 mutants.J Biol Chem. 280:2378-2387. no PMCID.

13. Shaffer KL, Sharma A, Snapp EL, Hegde RS. 2005. Regulation of protein compartmentalization expands the diversity of protein function. Dev Cell. 9:545-554. no PMCID.

14. Snapp EL. 2005. Membrane proteins modulate ER Organization. Proceedings of the 14th International Conference on Cytochromes P450: Biochemistry, Biophysics, and Bioinformatics. no PMCID.

15. Altan-Bonnet N, Sougrat R, Liu W, Snapp EL, Ward T, and Lippincott-Schwartz J. 2006. Golgi inheritance in mammalian cells is mediated through ER export activities. Mol Biol Cell. 17:990-1005. PMCID: PMC1356606.

16. Snapp EL, Sharma A,Lippincott-Schwartz J, and Hegde RS. 2006. Monitoring chaperone engagement of substrates in the endoplasmic reticulum of live cells. Proc Natl Acad Sci USA. 103:6536-6541. PMCID: PMC1458919.

17. Borgese N, Francolini M, and Snapp E. 2006. Endoplasmic Reticulum Architecture: Structures in Flux. Curr Op Cell Biol. 18:358-364. No PMCID.

18. Lippincott-Schwartz J and Snapp EL. 2006. Imaging of organelle membrane systems and membrane traffic in living cells. CSH Protoc.

19. Lippincott-Schwartz J and Snapp EL. 2006. Membrane trafficking and organelle reagents. CSH Protoc.

20. Kadereit B, Kumar P, Wang WJ, Miranda D, Snapp EL, Severina N, Torregroza I, Evans T, and Silver DL. 2007. An Evolutionarily conserved gene family is important for fat storage. Proc Natl Acad Sci USA. 105:94-99. PMCID: PMC2224239.

21. VanderHeyden AB, Naismith TV, Snapp EL, Hodzic D, Hanson PI, 2009. LULL1 retargets TorA to the nuclear envelope revealing an activity that is impaired by the DYT1 dystonia mutation. Mol Biol Cell. 20:2661-2672. PMCID: PMC2688546.

22. Ostrovsky O, Makarewich CA, Snapp EL, Argon Y. 2009. An essential role for ATP binding and hydrolysis in the chaperone activity of GRP94 in cells. Proc Natl Acad Sci USA. 106:11600-11605. PMCID: PMC2710619.

23. Snapp, EL. 2009. Fluorescent Proteins:  A Cell Biologist's User Guide. Trends Cell Biol. 19:649-55. PMCID: PMC2784028.

24. Muller L, Diaz de Ecuariaza M, Lajoie P, Theis M, Jung M, Muller A, Burgard C, Greiner M, Snapp EL, Dudek J, and Zimmerman R. 2010. Evolutionary gain of function for the ER membrane protein Sec62 from yeast to humans. Mol Biol Cell. 21:691-703 PMCID: PMC2828957.

25. Lai CW, Aronson D, and Snapp EL. 2010. BiP Availability Distinguishes States of Homeostasis and Stress in the Endoplasmic Reticulum of Living Cells. Mol Biol Cell. 21:1909-1921. PMCID: PMC2883936.

26. Gross DA, Snapp EL, and Silver D. 2010. Structural Insights into Triglyceride Storage Mediated by Fat-Storage-Inducing Transmembrane (FIT) Protein 2. PLoS ONE. 5(5): e10796. PMCID: PMC2875400

27. Benedix J, Lajoie P, Jaiswal H, Burgard C, Greiner M, Zimmerman R, Rospert S, Snapp EL, and Dudek J. 2010. BiP Modulates the Affinity of its Co-chaperone ERj1 to Ribosomes. J Biol Chem. 285:36427-36433. PMCID: PMC2978572.

28. Lajoie P and Snapp EL. 2010. Formation and toxicity of soluble Huntingtin oligomers in living cells. PLoS ONE. 5:e15245. PMCID: PMC3011017.

29. Matsuda S, Matsuda Y, Snapp EL, D'Adamio L. 2011. Maturation of BRI2 generates a specific inhibitor that reduces APP processing at the plasma membrane and in endocytic vesicles. Neurobiol Aging. 32:1400-1408. PMCID: PMC2932834.

30. Aronson DE, Costantini LM, and Snapp EL. 2011. Superfolder GFP is Fluorescent in Oxidizing Environments when Targeted via the Sec Translocon. Traffic. 12:543-548. PMCID: PMC3079558.

31. Howarth D, Vacaru A, Tsedensodnom O, Mormone E, Nieto N, Costantini L, Snapp EL, Sadler K. 2011. Alcohol disrupts endoplasmic reticulum function and protein secretion in hepatocytes. Alcoholism:  Clin Exp Res. PMCID: PMC3204333.

32. Lajoie P and Snapp EL. 2011. Changes in BiP availability reveal hypersensitivity to acute endoplasmic reticulum stress in cells expressing mutant Huntingtin. J Cell Sci. 124:3332-3343. PMCID: PMC3178454.

33. Vander Heyden AB, Naismith TV, Snapp EL, and Hanson PI. 2011. Monotopic membrane association mediates protein retention inside the endoplasmic reticulum. EMBO. 30:3217-3231. PMCID: PMC3160655.

34. Windsor M, Hawes P, Monaghan P, Snapp E, Salas ML, Rodriguez JM, and Wileman T. 2012. A Viral Structural Membrane Protein Induces Collapse of ER Membrane Cisternae during Assembly and Envelopment of African Swine Fever Virus. Traffic. 12:30-42. PMCID: PMC3237792.

35. Snapp EL and Lajoie P. 2011. Time-Lapse Imaging of Membrane Traffic in Living Cells. Cold Spring Harb Protoc. 2011 (11):1362-1365. PMCID in progress.

36. Snapp EL and Lajoie P. 2011. Photobleaching Regions of Living Cells to Monitor Membrane Traffic. Cold Spring Harb Protoc. 2011 (11): 1366-1367. PMCID in progress.

37. Snapp EL and Lajoie P. 2011. Activating Photoactivatable Proteins with Laser Light to Visualize Membrane Systems and Membrane Traffic in Living Cells. Cold Spring Harb Protoc. 2011 (11): 1368-1369. PMCID in progress.

38. Snapp EL and Lajoie P. 2011. Imaging of Membrane Systems and Membrane Traffic in Living Cells. Cold Spring Harb Protoc. 2011 (11): 1295-1304. PMCID in progress.

39. Kung LF, Pagant S, Futai E, D'Arcangelo J, Buchanan R, Dittmar JC, Reid RJD, Rothstein R, Hamamoto S, Snapp EL, Schekman R, and Miller EA. 2011. Sec24p and Sec16p cooperate to regulate the GTP cycle of the COPII coat. EMBO. 31:1014-1027. PMCID: PMC3280547

40. Lajoie P, Moir R, Willis I, and Snapp EL. 2012.Kar2p availability defines distinct forms of endoplasmic reticulum stress in living cells.Mol Biol Cell. 23:955-964. PMCID: PMC3290652.

41. Lai C*, Otero J*, Hendershot L, and Snapp EL. 2012. ERdj4 association with the ER membrane and ERAD machinery. J Biol Chem 287:7969-7978. PMC3318715. * These two authors contributed equally to this work.

42. Costantini L, Fossati M, Francolini M, and Snapp EL. 2012. A Quantitative Assay for Fluorescent Protein Oligomerization in Live Cells. Traffic. 13:643-649. PMC3324619.

43. Snapp EL. 2012. Unfolded Protein Responses With or Without Unfolded Proteins? Cells. 1(4):926-960. PMCID in progress. Review.

44. Ordonez A, Snapp EL, Tan L, Miranda E, Marciniak SJ, and Lomas DA. 2012. Endoplasmic reticulum polymers impair luminal protein mobility and sensitise to cellular stress in a (1)-antitrypsin deficiency. Hepatology. 57:2049-60. PMCID in progress.

45. Haataja L, Snapp E, Wright J, Liu M, Hardy AB, Wheeler MB, Markwardt ML, Rizzo M, and Arvan P. 2012. Proinsulin intermolecular interactions during secretory trafficking in pancreatic beta cells. J Biol Chem.288:1896-1906.PMC3548498.

46. Costantini LM, Subach O, Jaureguiberry-bravo M, Verkhusha V, and Snapp EL. 2012. Adapting a blue fluorescent protein for the secretory pathway. BBRC. 430:1114-1119. PMC3552020.

47. Guo F and Snapp EL. 2013. ERdj3 regulates BiP occupancy in cells. J Cell Sci. 126:1429-1439. PMCID: PMC3644143.

48. Costantini LM and Snapp EL. 2013. Fluorescent Proteins in Cellular Organelles:  Serious Pitfalls and Some Solutions. DNA Cell Biol. 32 (11):622-627. PMCID: PMC3806368. Journal cover.

49.Yuan F, Snapp EL, Novikoff PM, Suadicani SO, Spray DC, Potvin B, Wolkoff AW, Stanley P. 2014. Human Liver Cell Trafficking Mutants: Characterization and Whole Exome Sequencing. PLoS ONE. Jan 23;9(1):e87043. PMCID: PMC3900707.

50. Martinez MG, Snapp EL, Perumal GS, Macaluso FP, and Kielian M. 2014. Imaging the Alphavirus Exit Pathway. J Virol. 15:6922-6933. PMC4054368. Journal cover.

51. Lajoie P, Fazio EN, and Snapp EL. 2014. Approaches to imaging unfolded secretory protein stress in living cells. Endoplasmic Reticulum Stress in Diseases.1:27-39. PMC4238303

52. Clay L, Caudron F, Denoth-Lippuner A, Boettcher B, Snapp E, and Barral Y. 2014. A sphingolipid-dependent diffusion barrier confines ER stress to the yeast mother cell. eLife. 3:e01883. PMC4009826.

53. Hettich J, Ryan S, Norberto de Souz O, Saraiva Macedo Timmers L, Tsai S, Atai N, da Hora C, Zhang X, Kothary R, Calakos N, Snapp E, Ericsson M, Grundmann K, Breakefield, X, and Nery F. 2014. Biochemical and cellular analysis of human variants of the DYT1 dystonia protein, torsinA. Hum Mut. 35:1101-1113. PMC4134760

54. Ghosh R, Wang L, Wang ES, Gayani K. Perera B, Aeid I, Morita S, Prado K, Thamsen M, Caswell D, Macias H, Weiberth KF, Gliedt MJ, Alavi MV, Hari SB, Mitra AK, Bhhatarai B, Schurer SC, Snapp EL, Gould DB, German MS, Backes BJ, Maly DJ, Oakes SA, and Papa FR. 2014. Allosteric inhibition of the IRE1a RNase preserves cell viability and function during endoplasmic reticulum stress. Cell. 158:534-548. PMC4244221

55. Costantini LM, Irvin SC, Kennedy SC, Goldstein H, Herold BC, and Snapp EL. 2015. Engineering and exploitation of a fluorescent HIV-1 gp120 for live cell CD4 binding assays. Virology. 476:240-248. PMC4323844

56. D'Arcangelo JG, Crissman J, Pagant S, Copic S, Latham CF, Snapp EL, and Milller EA. 2015. Local concentration of p24 proteins and COPII coat composition mutually influence Sec13p-dependence and membrane scaffolding. Curr Biol. 25: 1296-1305. PMCID: PMC4439346

57. Costantini LM and Snapp EL. Going Viral with Fluorescent Proteins. 2014. Invited review for J Virology. 89:19 pp. .

58. Costantini L, Baloban M, Markwardt M, Guo F, Rizzo M, Verkhusha V, and Snapp EL. 2015. A palette of fluorescent proteins optimized for diverse cellular environments. Nature Comm. online. PMC4499870.


Book and Methods Chapters

1. Snapp EL, Altan N, and Lippincott-Schwartz J. 2003. Measuring protein mobility by photobleaching GFP-chimeras in living cells. Unit 21.1: Bonifacino, J., Dasso, M., Harford, J., Lippincott-Schwartz, J., Yamada, K. editors. Morgan, K. S. series editor. in Current Protocols in Cell Biology. John Wiley & Sons, Inc. New York. no PMCID.

2. Snapp EL. 2004. ER biogenesis:  proliferation and differentiation. The Biogenesis of Cellular Organelles. Molecular Biology Intelligence Unit. ed. Mullins, C. Landes Bioscience. Georgetown, TX. Kluwer Academic/Plenum Publishers. New York, NY. pp.63-95.

3. Lippincott-Schwartz J and Snapp EL. 2004. Imaging of membrane systems and membrane traffic in living cells. eds. Goldman, R. and Spector, D. Live Cell Imaging: A Laboratory Manual.Cold Spring Harbor Press. Cold Spring Harbor, NY.

4. Snapp EL. 2005. Design and Use of Fluorescent Fusion Proteins in Cell Biology. Unit 21.4. Bonifacino, J., Dasso, M., Harford, J., Lippincott-Schwartz, J., Yamada, K. editors. Morgan, K. S. series editor. In Current Protocols in Cell Biology. John Wiley & Sons, Inc. New York. PMCID: PMC2875081

5. Snapp EL and Hegde RS. 2006. Rational design and evaluation of FRET experiments to measure protein proximities in cells. Bonifacino, J., Dasso, M., Harford, J., Lippincott-Schwartz, J., Yamada, K. editors. Morgan, K. S. series editor. In Current Protocols in Cell Biology. John Wiley & Sons, Inc. New York. PMCID: PMC2875078

6. Snapp EL. 2006. Photobleaching Methods. Encyclopedic Reference of Genomics and Proteomics in Molecular Medicine. ed. Oschkinat, H. and Schieder, P. Springer Verlag. Heidelberg.

7. Aronson DE and Snapp EL. 2009. Translocon Organization in Cells. Translocon. Zimmerman R. editor. in Protein Transport into the Endoplasmic Reticulum. Landes Bioscience. Georgetown, TX. Kluwer Academic/Plenum Publishers. New York, NY.

8. Snapp EL. 2009. Imaging Cellular Proteins and Structures:  Smaller, Brighter, and Faster. In The Liver:  Biology and Pathobiology. Wolkoff AW, Fausto N, Boyer J, Shafritz D, Arias I, and Cohen DE. editors. Blackwell Pulbishing, Oxford UK.

9. Lajoie P and Snapp EL. 2010. Imaging of membrane systems and membrane traffic in living cells. eds. Goldman, R. and Spector, D. Live Cell Imaging: A Laboratory Manual. Second Edition.Cold Spring Harbor Press. Cold Spring Harbor, NY.

10. Lajoie P and Snapp EL. 2013. Detecting Soluble polyQ Oligomers and Investigating Their Impacts on Living Cells Using Split-GFP. eds Hatters DM and Hannan AJ. Tandem Repeats in Genes, Proteins, and Disease:  Methods and Protocols (Methods in Molecular Biology). Humana Press. 1017:229-239.

11. Costantini LM and Snapp EL. Photobleaching Analysis of the Endoplasmic Reticulum. 2013. Bonifacino, J., Dasso, M., Harford, J., Lippincott-Schwartz, J., Yamada, K. editors. Morgan, K. S. series editor. In Current Protocols in Cell Biology. John Wiley & Sons, Inc. New York. in press

12. Snapp EL. 2013.Photobleaching Methods to study Golgi Complex Dynamics in Living Cells. Methods for Analysis of Golgi Complex Function, edited by Franck Perez and David Stephens. Methods in Cell Biology. in press.



1. Francolini M, Snapp EL, Borgese N. Organized smooth endoplasmic reticulum. ASCB Image & Video Library. May 2007:CYT-81. (http://cellimages.ascb.org/u?/p4041coll7,124)



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