Steve Briggs

Research

We study molecular signaling networks with a focus on the innate immune system of plants. To support our studies, we developed a proteomics capability that is sensitive enough to discover new genes and gene models (1); discover genes based solely on comparison between the proteomes of mutant and wild type plants (2), and discover mechanisms of signaling mediated by protein phosphorylation (3). We used mass spectrometry to generate a proteomics atlas, elements of which have been published (4, 5, 6). When combined with RNA-seq data, our integrated gene expression atlas was used to derive co-expression networks and gene regulatory networks from the proteome and transcriptome alone and from integration of the data. We found that the transcriptome does not predict the proteome either quantitatively or qualitatively (4) and networks derived from protein levels have little overlap with networks of the same genes measured according to their mRNA levels (7). Recent reports on host-microbe interactions include studies of host peptide signaling (8), pathogen effector secretion (9, 10), self-acetylation of host proteins caused by a pathogen effector (11), and biosynthesis of defense metabolites in response to infection (12). We collaborate with other labs to understand problems in signaling that are less central to our interests but that can be uniquely addressed using our expertise. These include understanding endoplasmic reticulum stress (13, 14) and circadian signaling in plants (15); chemotactic signaling in Dictyostelium (16, 17); and the molecular determinants of chronic lymphocytic leukemia (18, 19).

  1. Castellana NE, Shen Z, He Y, Walley JW, Cassidy CJ, Briggs SP, Bafna V. An Automated Proteogenomic Method Uses Mass Spectrometry to Reveal Novel Genes in Zea mays. Mol Cell Proteomics. 2014 Jan;13(1):157-67. doi: 10.1074/mcp.M113.031260.
  2. Zhang X, Facette M, Humphries JA, Shen Z, Park Y, Sutimantanapi D, Sylvester AW, Briggs SP, Smith LG. Identification of PAN2 by quantitative proteomics as a leucine-rich repeat-receptor-like kinase acting upstream of PAN1 to polarize cell division in maize. Plant Cell. 2012 Nov;24(11):4577-89. doi: 10.1105/tpc.112.104125. Epub 2012 Nov 21. PubMed PMID: 23175742; PubMed Central PMCID: PMC3531853.
  3. Qiao H, Shen Z, Huang SS, Schmitz RJ, Urich MA, Briggs SP, Ecker JR. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science. 2012 Oct 19;338(6105):390-3. doi: 10.1126/science.1225974. Epub 2012 Aug 30. PubMed PMID: 22936567; PubMed Central PMCID: PMC3523706.
  4. Walley JW, Shen Z, Sartor R, Wu KJ, Osborn J, Smith LG, Briggs SP. Reconstruction of protein networks from an atlas of maize seed proteotypes. Proc Natl Acad Sci U S A. 2013 Dec 3;110(49):E4808-17. doi: 10.1073/pnas.1319113110. Epub 2013 Nov 18. PubMed PMID: 24248366; PubMed Central PMCID: PMC3856832.
  5. Facette MR, Shen Z, Björnsdóttir FR, Briggs SP, Smith LG. Parallel proteomic and phosphoproteomic analyses of successive stages of maize leaf development. Plant Cell. 2013 Aug;25(8):2798-812. doi: 10.1105/tpc.113.112227. Epub 2013 Aug 9. PubMed PMID: 23933881; PubMed Central PMCID: PMC3784581.
  6. Marcon C, Malik WA, Walley JW, Shen Z, Paschold A, Smith LG, Piepho HP, Briggs SP, Hochholdinger F. A high resolution tissue-specific proteome and phosphoproteome atlas of maize primary roots reveals functional gradients along the root axis. Plant Physiol. 2015 Mar 16. pii: pp.00138.2015
  7. Walley JW, Sartor RC, Shen Z, Schmitz RJ, Wu KJ, Urich MA, Nery JR, Smith LG, Schnable JC, Ecker JR, Briggs SP. Integration of omic networks in a developmental atlas of maize. 2016 Science. Aug 19;353(6301):814-8. doi: 10.1126/science.aag1125. PMID: 27540173
  8. Huffaker A, Pearce G, Veyrat N, Erb M, Turlings TC, Sartor R, Shen Z, Briggs SP, Vaughan MM, Alborn HT, Teal PE, Schmelz EA. Plant elicitor peptides are conserved signals regulating direct and indirect antiherbivore defense. Proc Natl Acad Sci U S A. Apr 2;110(14):5707-12. doi: 10.1073/pnas.1214668110. 2013
  9. Chaudhary R, Atamian HS, Shen Z, Briggs SP, Kaloshian I. Potato aphid salivary proteome: enhanced salivation using resorcinol and identification of aphid phosphoproteins. J Proteome Res. 2015 Apr 3;14(4):1762-78. doi: 10.1021/pr501128k.
  10. Chaudhary R, Atamian HS, Shen Z, Briggs SP, Kaloshian I. GroEL from the endosymbiont Buchnera aphidicola betrays the aphid by triggering plant defense. Proc Natl Acad Sci U S A. 2014 Jun 17;111(24):8919-24. doi: 10.1073/pnas.1407687111.
  11. Walley JW, Shen Z, McReynolds MR, Schmelz EA, Briggs SP. Fungal-induced protein hyperacetylation in maize identified by acetylome profiling. 2018 Proc Natl Acad Sci U S A. Jan 2;115(1):210-215. doi:10.1073/pnas.1717519115. Epub 2017 Dec 19. PMID: 29259121
  12. Mafu S, Ding Y, Murphy KM, Yaacoobi O, Addison JB, Wang Q, Shen Z, Briggs SP, Bohlmann J, Castro-Falcon G, Hughes CC, Betsiashvili M, Huffaker A, Schmelz EA, Zerbe P. 2018 Discovery, Biosynthesis and Stress-Related Accumulation of Dolabradiene-Derived Defenses in Maize. Plant Physiol. Apr;176(4):2677-2690. doi: 10.1104/pp.17.01351. Epub 2018 Feb 23. PMID: 29475898
  13. Wang JZ, Li B, Xiao Y, Ni Y, Ke H, Yang P, de Souza A, Bjornson M, He X, Shen Z, Balcke GU, Briggs SP, Tissier A, Kliebenstein DJ, Dehesh K. 2017 Initiation of ER Body Formation and Indole Glucosinolate Metabolism by the Plastidial Retrograde Signaling Metabolite, MEcPP. Mol Plant. Nov 6;10(11):1400-1416. doi:10.1016/j.molp.2017.09.012. Epub 2017 Sep 28. PMID: 28965830
  14. Walley J, Xiao Y, Wang JZ, Baidoo EE, Keasling JD, Shen Z, Briggs SP, Dehesh K. Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proc Natl Acad Sci U S A. 2015 May 12;112(19):6212-7. doi: 10.1073/pnas.1504828112. Epub 2015 Apr 28. PubMed PMID: 25922532; PubMed Central PMCID: PMC4434691.
  15. Huang H, Alvarez S, Bindbeutel RK, Shen Z, Naldrett MJ, Evans BS, Briggs SP, Hicks LM, Kay SA, Nusinow DA. Identification of evening complex associated proteins in Arabidopsis by affinity purification and mass spectrometry. Mol Cell Proteomics. 2015 Nov 6. pii: mcp.M115.054064
  16. Lacal Romero J, Shen Z, Baumgardner K, Wei J, Briggs SP, Firtel RA. The Dictyostelium GSK3 kinase GlkA coordinates signal relay and chemotaxis in response to growth conditions. 2018 Dev Biol. Mar 1;435(1):56-72.doi: 10.1016/j.ydbio.2018.01.007. Epub 2018 Jan 20. PMID: 29355521
  17. Khanna A, Lotfi P, Chavan AJ, Montaño NM, Bolourani P, Weeks G, Shen Z, Briggs SP, Pots H, Van Haastert PJ, Kortholt A, Charest PG. 2016 The small GTPases Ras and Rap1 bind to and control TORC2 activity. Sci Rep. May 13;6:25823. doi: 10.1038/srep25823. PMID: 27172998
  18. Hasan MK, Yu J, Widhopf GF 2nd, Rassenti LZ, Chen L, Shen Z, Briggs SP, Neuberg DS, Kipps TJ. Wnt5a induces ROR1 to recruit DOCK2 to activate Rac1/2 in chronic lymphocytic leukemia. 2018 Blood. Jul 12;132(2):170-178. doi: 10.1182/blood-2017-12-819383. Epub 2018 Apr 20. PMID: 29678828May 3. PMID: 284655282016
  19. Yu J, Chen L, Cui B, Widhopf GF 2nd, Shen Z, Wu R, Zhang L, Zhang S, Briggs SP, Kipps TJ. Wnt5a induces ROR1/ROR2 hetero-oligomerization to enhance leukemia chemotaxis and proliferation. J Clin Invest. 2015 Dec 21. pii: 83535. doi: 10.1172/JCI83535.

Select Publications

  • Walley JW, Shen Z, McReynolds MR, Schmelz EA, Briggs SP. Fungal-induced protein hyperacetylation in maize identified by acetylome profiling. Proc Natl Acad Sci U S A. Jan 2;115(1):210-215. doi:10.1073/pnas.1717519115. Epub 2017 Dec 19. PMID: 29259121
  • Mafu S, Ding Y, Murphy KM, Yaacoobi O, Addison JB, Wang Q, Shen Z, Briggs SP, Bohlmann J, Castro-Falcon G, Hughes CC, Betsiashvili M, Huffaker A, Schmelz EA, Zerbe P. Discovery, Biosynthesis and Stress-Related Accumulation of Dolabradiene-Derived Defenses in Maize. Plant Physiol. Apr;176(4):2677-2690. doi: 10.1104/pp.17.01351. Epub 2018 Feb 23. PMID: 29475898
  • Lacal Romero J, Shen Z, Baumgardner K, Wei J, Briggs SP, Firtel RA. The Dictyostelium GSK3 kinase GlkA coordinates signal relay and chemotaxis in response to growth conditions. Dev Biol. Mar 1;435(1):56-72.doi: 10.1016/j.ydbio.2018.01.007. Epub 2018 Jan 20. PMID: 29355521
  • Hasan MK, Yu J, Widhopf GF 2nd, Rassenti LZ, Chen L, Shen Z, Briggs SP, Neuberg DS, Kipps TJ. Wnt5a induces ROR1 to recruit DOCK2 to activate Rac1/2 in chronic lymphocytic leukemia. Blood. Jul 12;132(2):170-178. doi: 10.1182/blood-2017-12-819383. Epub 2018 Apr 20. PMID: 29678828May 3. PMID: 28465528
  • Hasan MK, Yu J, Chen L, Cui B, Widhopf Ii GF, Rassenti L, Shen Z, Briggs SP, Kipps TJ. Wnt5a induces ROR1 to complex with HS1 to enhance migration of chronic lymphocytic leukemia cells. Leukemia. Dec;31(12):2615-2622. doi: 10.1038/leu.2017.133. Epub 2017 May 3. PMID: 28465529
  • Marcon C, Malik WA, Walley JW, Shen Z, Paschold A, Smith LG, Piepho HP, Briggs SP, Hochholdinger F. A high resolution tissue-specific proteome and phosphoproteome atlas of maize primary roots reveals functional gradients along the root axis. Plant Physiol. 2015 Mar 16. pii: pp.00138.2015
  • Yu J, Chen L, Chen Y, Hasan MK, Ghia EM, Zhang L, Wu R, Rassenti LZ, Widhopf GF, Shen Z, Briggs SP, Kipps TJ. Wnt5a induces ROR1 to associate with 14-3-3ζ for enhanced chemotaxis and proliferation of chronic lymphocytic leukemia cells. Leukemia. Dec;31(12):2608-2614. doi: 10.1038/leu.2017.132. Epub 2017 May 3. PMID: 28465528
  • Wang JZ, Li B, Xiao Y, Ni Y, Ke H, Yang P, de Souza A, Bjornson M, He X, Shen Z, Balcke GU, Briggs SP, Tissier A, Kliebenstein DJ, Dehesh K. Initiation of ER Body Formation and Indole Glucosinolate Metabolism by the Plastidial Retrograde Signaling Metabolite, MEcPP. Mol Plant. Nov 6;10(11):1400-1416. doi:10.1016/j.molp.2017.09.012. Epub 2017 Sep 28. PMID: 28965830
  • Walley JW, Sartor RC, Shen Z, Schmitz RJ, Wu KJ, Urich MA, Nery JR, Smith LG, Schnable JC, Ecker JR, Briggs SP. Integration of omic networks in a developmental atlas of maize. Science. Aug 19;353(6301):814-8. doi: 10.1126/science.aag1125. PMID: 27540173
  • Khanna A, Lotfi P, Chavan AJ, Montaño NM, Bolourani P, Weeks G, Shen Z, Briggs SP, Pots H, Van Haastert PJ, Kortholt A, Charest PG. The small GTPases Ras and Rap1 bind to and control TORC2 activity. Sci Rep. May 13;6:25823. doi: 10.1038/srep25823. PMID: 27172998
  • Yu J, Chen L, Cui B, Widhopf GF 2nd, Shen Z, Wu R, Zhang L, Zhang S, Briggs SP, Kipps TJ. Wnt5a induces ROR1/ROR2 heterooligomerization to enhance leukemia chemotaxis and proliferation. J Clin Invest. Feb;126(2):585-98. PMID: 26690702
  • Huang H, Alvarez S, Bindbeutel RK, Shen Z, Naldrett MJ, Evans BS, Briggs SP, Hicks LM, Kay SA, Nusinow DA. Identification of evening complex associated proteins in Arabidopsis by affinity purification and mass spectrometry. Mol Cell Proteomics. Jan;15(1):201-17. doi: 10.1074/mcp.M115.054064. Epub 2015 Nov 6. PMID: 26545401
  • Marcon C, Malik WA, Walley JW, Shen Z, Paschold A, Smith LG, Piepho HP, Briggs SP, Hochholdinger F. A high-resolution tissue-specific proteome and phosphoproteome atlas of maize primary roots reveals functional gradients along the root axes. Plant Physiol. May;168(1):233-46. doi: 10.1104/pp.15.00138. Epub 2015 Mar 16. PubMed PMID: 25780097; PubMed Central PMCID: PMC4424028.
  • Yu J, Chen L, Cui B, Widhopf GF 2nd, Shen Z, Wu R, Zhang L, Zhang S, Briggs SP, Kipps TJ. Wnt5a induces ROR1/ROR2 heterooligomerization to enhance leukemia chemotaxis and proliferation. J Clin Invest. Dec 21. pii: 83535. doi: 10.1172/JCI83535.
  • Nakasaki M, Hwang Y, Xie Y, Kataria S, Gund R, Hajam EY, Samuel R, George R, Danda D, M J P, Nakamura T, Shen Z, Briggs S, Varghese S, Jamora C. The matrix protein Fibulin-5 is at the interface of tissue stiffness and inflammation in fibrosis. Nat Commun. Oct 15;6:8574. doi: 10.1038/ncomms9574.
  • Pineda G, Shen Z, Ponte de Albuquerque C, Reynoso E, Chen J, Tu C-C, Tang W, Briggs S, Zhou H, Wang JY. Proteomics Studies of the Interactome of RNA Polymerase II C-Terminal Repeated Domain. BMC Research Notes Oct 29;8:616. doi: 10.1186/s13104-015-1569-y
  • Walley J, Xiao Y, Wang J-Z, Baidoo EE, Keasling JD, Shen Z, Briggs SP, Dehesh K. Plastid-produced interorgannellar stress signal MEcPP potentiates induction of the unfolded protein response in endoplasmic reticulum. Proc Natl Acad Sci USA April 28, doi: 10.1073/pnas.1504828112
  • Xiong J, Todorova D, Su NY, Kim J, Lee PJ, Shen Z, Briggs SP, Xu Y. Stemness factor Sall4 is required for DNA damage response in embryonic stem cells. J Cell Biol. Mar 2;208(5):513-20. doi: 10.1083/jcb.201408106.
  • Chaudhary R, Atamian HS, Shen Z, Briggs SP, Kaloshian I. Potato aphid salivary proteome: enhanced salivation using resorcinol and identification of aphid phosphoproteins. J Proteome Res. Apr 3;14(4):1762-78. doi: 10.1021/pr501128k.

Biography

Briggs earned his Ph.D. from Michigan State University and spent the first half of his career in industry as Director at Pioneer/DuPont; President of Torrey Mesa Research Institute; and Senior Vice President for Corporate Research at Diversa. He served as Senior Staff Investigator at Cold Spring Harbor Laboratory. Briggs joined the faculty at UCSD as Professor where he served as Chair of the Section of Cell & Developmental Biology, Associate Dean of the Division of Biology, and Interim Chair of the Department of Chemistry and Biochemistry. He is a member of the National Academy of Sciences, a Fellow of the American Association for the Advancement of Science, and a Fellow of the National Academy of Inventors.