Sathyanarayanan Puthanveettil, PhD

Associate Professor
Department of Neuroscience
Florida Campus



Scripps Research Joint Appointments

Faculty, Graduate Program

Research Focus

Molecular Logic For The Storage and Maintenance Of Long-Term Memory

The long-term goal of my laboratory is to understand the molecular and cellular basis of memory storage and cognitive disorders. At the cellular level there are two hallmarks of long-term memory storage: experience-dependent activation of gene expression in the nucleus, and local activation of translation at specific synapses. 

Previously I have demonstrated in Eric Kandel’s laboratory that activation of fast axonal transport in pre- and post- synaptic neurons during learning is another critical component of long-term memory storage. Activation of molecular transport to synapses is a rate limiting step and coordinates nuclear and synaptic processes during memory storage. The transported cargos include organelles, proteins, mRNAs, and noncoding RNAs. 

In an effort to learn what gene products are transported in specific neurons in response to activity, how they are transported, how they are stored for later use, and eventually when and how they are utilized at specific synapses during learning and memory storage, my laboratory uses an integrated approach that combines several high throughput techniques such as genomics and proteomics with electrophysiology, biochemistry, and imaging. A comprehensive understanding of transported cargos will help us in elucidating signaling pathways at the synapse and mechanisms underlying synaptic dysfunction. Animal models such as Aplysia and mice are used to tackle these questions at the cellular and systems levels. In addition, we explore these questions using mouse models for cognitive disorders such as Alzheimer’s and Huntington’s disease.


Education

B.S., Biology, Kerala Agricultural University,
Ph.D., Biology, Washington State University,
M.S., Biotechnology, Tamil Nadu Agricultural University,

Professional Experience

1994-1996       Research Assistant, International Center for Genetic Engineering and
                       Biotechnology (ICGEB), United Nations Industrial
                       Developmental Organization, New Delhi, India
1995-1996       Visiting Scientist. Rice Genome Research Program, STAFF Institute.
                       Tsukuba, Japan.
1996-2001       Graduate Research Assistant. Poovaiah laboratory, Washington State
                       University, Pullman.
2001-2006       HHMI Research Associate/Postdoctoral Research Scientist,
                       Eric Kandel Laboratory, Columbia University Medical Center   
2006                Associate Research Scientist, Eric Kandel Laboratory,
                       Columbia University Medical Center
2010 - 2014     Assistant Professor, Department of Neuroscience, Scripps Florida
2011                Faculty member, Kellog School of Science and Technology,
                       The Scripps Research Institute
                       Adjunct faculty, Department of Biological Sciences,
                       Florida Atlantic University.
                       Adjunct faculty, Department of Biomedical Sciences,
                       Charles E. Schmidt School of Medicine, FAU                                  
2015 -              Associate Professor, Department of Neuroscience, Scripps Research

Awards & Professional Activities

1984 - 1991    National Merit Scholarship, Department of Education, India
1997              Cold Spring Harbor Laboratory Registration waiver
2000              Gordon Research Conference Chair’s Funds for Registration Fees
2000              Washington State University (WSU) Graduate School Travel Award
2000              American Society for Gravitational and Space Biology (ASGSB)
                     Travel Grant
2003              The National Neurofibromatosis Foundation and International
                     Neurofibromatosis Research Foundation Prize for Innovative
                     Research Ideas
2009              Cold Spring Harbor Laboratory Registration Waiver  
2009              Society For Neuroscience (SFN) recognized my work on Kinesin
                     transported RNAs as “HOT TOPIC” for Neuroscience 2009
2010              Columbia University Nominee for Blavatnik Award of
                     New York Academy of Sciences
2011              Margaret Q. Landenberger Research Foundation
                     Young Investigator Award
2011              TSRI Nomineee for Alfred Sloan Award, Searle Scholar Award.
2012              Whitehall Foundation Award
2015              National Science Foundation CAREER Award

Selected References

Rizzo V, Touzani K, Raveendra, BL, Swarnkar S, Lora J, Kadakkuzha BM, Liu XA, Zhang C, Betel D, Stackman RW, Puthanveettil SV. (2016) Encoding of contextual fear memory requires de novo proteins in the prelimbic cortex. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging. Published online, http://dx.doi.org/10.1016/j.bpsc.2016.10.002  PMID:28503670

Miller KE, Liu XA, Puthanveettil SV. (2015) Automated measurement of fast mitochondrial transport in neurons. Front Cell Neurosci. 9:435.  PMID: 26578890  PMCID:PMC4630299

Rumbaugh G, Sillivan SE, Ozkan ED, Rojas CS, Hubbs CR, Aceti M, Kilgore M, Kudugunti S, Puthanveettil SV, Sweatt JD, Rusche J, Miller CA. (2015). Pharmacological selectivity within class I histone deacetylases predicts effects on synaptic function and memory rescue. Neuropsychopharmacology. doi:10.1038/npp.2015.93.  PMID: 25837283  PMCID:PMC4538358

Kadakkuzha BM, Liu XA, Shankar G, McCrate J, Afinogenova A, Young B, Rizzo A, Fallahi M, Raveendra B, Puthanveettil SV. (2015). Transcriptome analysis reveal enrichment of specific lncRNAs in specific brain regions and neuronal populations. Front Cell Neurosci. 9:63.  PMID: 25798087  PMCID:PMC4351618

Rizzo V, Richman J, Puthanveettil SV. (2014). Dissecting mechanisms of brain aging by studying the intrinsic excitability of neurons. Frontiers in Aging Neuroscience. doi:10.3389/fnagi.2014.00337.  PMID: 25610394  PMCID:PMC4285138

Kadakkuzha BM, Spicer TP, Chase P, Richman JB, Hodder P, Puthanveettil SV. (2014). High-throughput screening for small molecule modulators of motor protein Kinesin. Assay Drug Dev Technol.12:470-80. doi: 10.1089/adt.2014.579.  PMID: 25383721

Liu XA, Kadakkuzha B, Pascal B, Steckler C, Akhmedov K, Yan L, Chalmers M, Puthanveettil SV. (2014) New approach to capture and characterize synaptic proteome. Proc Natl Acad Sci U S A. 2014 Nov 11;111:16154-9. doi: 10.1073/pnas.1401483111.  PMID: 25352669  PMCID:PMC4234550

Kadakkuzha BM, Liu XA, Narvaez M, Akhmedov K, *Puthanveettil SV. (2014) Asymmetric localization of natural antisense RNA of neuropeptide sensorin in Aplysia sensory neurons during aging and activity. Front Genet. 5:84.  PMID: 24795747  PMCID:PMC4001032

Choi YB, Kadakkuzha BM, Liu XA, Akhmedov K, *Kandel ER, *Puthanveettil SV. (2014) Huntingtin is critical both pre- and postsynaptically for long-term learning-related synaptic plasticity in aplysia. PLoS One. 9:e103004.  PMID: 25054562  PMCID:PMC4108396

Akhmedov K, Rizzo V, Kadakkuzha BM, Capo T, *Puthanveettil SV. (2013) Decreased response to acetylcholine during aging of Aplysianeurons R15. PLoS One. DOI: 10.1371/journal.pone.0084793.  PMID:24386417  PMCID:PMD3874043

Akhmedov K, Kadakkuzha BM, Puthanveettil SV. (2013) Aplysia ganglia preparation for electrophysiological and molecular analyses of single neurons. The Journal of Visualized Experiments (JoVE). e51075, doi:10.3791/51075.  PMID: 24457225  PMCID:PMC4089395

Puthanveettil, SV (2013) RNA transport and long-term memory storage. RNA Biol. 10:1765-70.  PMID: 24356491  PMCID:PMC3917979

Kadakkuzha, BM, Akhmedov, K, Capo, TR, Carvalloza, AC, Fallahi, M, Puthanveettil, SV (2013) Age-associated bidirectional modulation of gene expression in single identified R15 neuron of Aplysia. BMC Genomics. 14:880.  PMID: 24330282  PMCID:PMC3909179

Kadakkuzha BH and Puthanveettil SV. (2013) Genomics and proteomics in solving brain complexity. Mol Biosyst. 9:1807-1821.  PMID: 23615871 

Puthanveettil SV, Antonov I, Kalachikov S, Rajasethupathy P, Choi Y.B, Kohn AB, Citarella M, Yu F, Kar, KA, Kinet M, Morozova I, Russo JJ, Ju J, Moroz LL, Kandel ER. (2013) A strategy to capture and characterize the synaptic transcriptome. Proc Natl Acad Sci USA. 110:7464-7469.  PMID: 23589870  PMCID:PMC3645558

Raveendra BL, Siemer A, Puthanveettil SV, Hendrickson WA, McDermot A, Kandel ER. (2013) Characterization of prion-like conformational changes of the neuronal isoform of Aplysia CPEB. Nat Struct Mol Biol. 20:495-501.  PMID: 23435381  PMCID:PMC5518672

Liu XA, Rizzo V, Puthanveettil SV. (2012) Pathologies of axonal transport in neurodegenerative diseases. Trans Neurosci. 3:355-372.    PMID: 23750323  PMCID:PMC3674637

Jin I, Puthanveettil SV, Udo H, Karl K, Kandel ER, Hawkins RD. (2012) Spontaneous transmitter release is critical for the induction of long-term and intermediate-term facilitation in Aplysia. Proc Natl Acad Sci USA. 109:9131-6. PMCID: 22619333 PMCID:PMC3384218

Jin I, Udo H, Rayman JB, Puthanveettil SV, Vishwasrao HD, Kandel ER, Hawkins RD. (2012) Spontaneous transmitter release recruits postsynaptic mechanisms of long-term and intermediate-term facilitation in Aplysia. Proc Natl Acad Sci USA. 109:9137-9142.  PMID: 22619333 PMCID:PMC3384218

Choi YB, Kassabov SR, Jin I, Puthanveettil SV, Karl KA, Lu Y, Kim JH, Bailey CH, Kandel ER. (2011) Neurexin-neuroligin transsynaptic interaction mediates learning-related synaptic remodeling and long-term facilitation in Aplysia. Neuron. 70:468-481.  PMID: 21555073  PMCID:PMC3136118

Puthanveettil SV and Kandel ER. (2011).  Molecular mechanisms of initiation and maintenance of long-term memory storage.  T. Curran and Y. Christen (eds.), Two Faces of Evil: Cancer and Neurodegeneration, Research and Perspectives in Alzheimer's Disease.  DOI 10.1007/978-3-642-16602-0_13, Springer-Verlag Berlin Heidelberg.

Book Chapter: Du L, Yang T, Puthanveettil SV, and Poovaiah BW. (2011).  Decoding of Calcium Signal through Calmodulin: Calmodulin-binding Proteins in Plants.  Edited by Sheng Luan, University of California, Berkeley. Pgs 177-235.

Rajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S. V., E. Russo, J. R., Sander, S., Tuschl, T., and Kandel, E.R. (2009) Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining long-term synaptic plasticity through CREB. Neuron. 63:803-17.

Puthanveettil, S. V., Monje, F. J., Miniaci, M. C., Choi, Y. B., Karl, K. A., Khandros, E., Gawinowicz, M. A., Sheetz, M. P., and Kandel, E. R. (2008) A new component in synaptic plasticity: upregulation of kinesin in the neurons of the gill-withdrawal reflex. Cell. 135:960-73. * Faculty of 1000 evaluated "Must read" paper in Neuroscience

Miniaci, M. C., Kim, J. H., Puthanveettil, S. V., Si, K., Zhu, H., Kandel, E. R., Bailey, C. H. (2008) Sustained CPEB-dependent local protein synthesis is required to stabilize synaptic growth for persistence of long-term facilitation in Aplysia. Neuron. 59:1024-36.

Touzani, K., Puthanveettil, S. V., and Kandel, E. R. (2007) Consolidation of learning strategies during spatial working memory task requires proteins synthesis in the prefrontal cortex. Proceedings of the National Academy of Sciences (PNAS). 104:5632-7.

Marti AA, Li X, Jockusch S, Li Z, Raveendra B, Kalachikov S, Russo JJ, Morozova I, Puthanveettil SV, Ju J, Turro NJ. (2006) Pyrene binary probes for unambiguous detection of mRNA using time-resolved fluorescence spectroscopy. Nucleic Acids Res. 34:3161-3168.  PMID: 16769776  PMCID:PMC1477857

*Moroz LL, *Edwards JR, *Puthanveettil SV, *Kohn AB, Ha T, Heyland A, Knudsen B, Sahni A, Yu F, Liu L, Jezzini S, Lovell P, Iannucculli W, Chen M, Nguyen T, Sheng H, Shaw R, Kalachikov S, Panchin YV, Farmerie W, Russo JJ, Ju J and Kandel ER. (2006) Neuronal transcriptome of aplysia: neuronal compartments and circuitry. Cell. 127:1453-1467. *equal contributor * Faculty of 1000 evaluated.  PMID: 17190607  PMCID:PMC4024467

Sathyanarayanan PV and Poovaiah BW. (2004) Decoding Ca2+ signals in plants. CRC Crit Rev Plant Sciences. 23:1-11.  PMID: 16044584

Sathyanarayanan PV and Poovaiah BW. (2002) Autophosphorylation-dependent inactivation of plant chimeric calcium/calmodulin dependent protein kinase. Eur J Biochem. 269:2457-2463.  PMID: 12027883

Sathyanarayanan PV, Siems WF, Jones JP and Poovaiah BW. (2001) Calcium-stimulated autophosphorylation site of plant chimeric calcium/calmodulin-dependent protein kinase. J Biol Chem. 276:32940-32947.  PMID:11399751

Sathyanarayanan PV, Cremo CR and  Poovaiah BW. (2000) Plant chimeric Ca2+ /Calmodulin -dependent protein kinase. Role of the neural visinin-like domain in regulating autophosphorylation and calmodulin binding affinity. J Biol Chem. 275:30417-30422.  PMID: 10840028

Poovaiah BW, Xia M, Liu Z, Wang W, Yang T, Sathyanarayanan, PV and Franceschi VR. (1999) Developmental regulation of the gene for chimeric calcium/calmodulin-dependent protein kinase in anthers. Planta. 209:161-171.  PMID: 10436217

Mohan, M., Sathyanarayanan, P. V., Kumar, A., Srivastava, M. N., and Nair. S (1997) Molecular mapping of a resistance-specific PCR-based marker linked to a gall midge resistance gene (Gm4t) in rice. Theoretical and Applied Genetics. 95: 777-782.

Reddy AR, Scheffler B, Madhuri G, Srivastava MN, Kumar A, Sathyanarayanan PV, Nair S and Mohan M. (1996) Chalcone synthase in rice (Oryza sativa L.): detection of the CHS protein in seedlings and molecular mapping of the chs locus. Plant Mol Biol.  32:735-743.  PMID: 8980525


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