Foundational materials

Reading and Writing the Morphogenetic Code
Foundational White Paper of the Allen Discovery Center at Tufts University


61. L-type voltage-gated Ca2+ channel CaV1.2 regulates chondrogenesis during limb development
Atsuta, Y., Tomizwa, R. R., Levin, M., and Tabin, C. J.
PNAS, in press

60. Bioelectric control of metastasis in solid tumors
Payne, S. L., Levin, M., and Oudin, M. J.
Bioelectricity, 1(3): 114-130

59. Morphological coordination: unifying neural and non-neural signaling
Fields, C., Bischof, J., and Levin, M.
Physiology, in press

58. Bioelectrical controls of morphogenesis: from ancient mechanisms of cell coordination to biomedical opportunities
Whited, J., and Levin, M.
Current Opinion in Genetics & Development, 57: 61-69

57. From non-excitable single-cell to multicellular bioelectrical states supported by ion channels and gap junction proteins: electrical potentials as distributed controllers
Cervera, C., Pai, V. P., Levin, M., and Mafe, S.
Progress in Biophysics and Molecular Biology, in press

56. Morphogenesis as Bayesian Inference: a Variational Approach to Pattern Formation and Control in Complex Biological Systems
Kuchling, F., Friston, K., Georgiev, G., and Levin, M.
Physics of Life Reviews, in press

55. Mechanisms of physiological tissue remodeling in animals: Manipulating tissue, organ, and organism morphology
Pinet K, McLaughlin KA.
Dev Biol., 2019 Apr 8. pii: S0012-1606(18)30759-0. doi: 10.1016/j.ydbio.2019.04.001 [cover]

54. Recovery of the Xenopus laevis heart from ROS-induced stress utilizes conserved pathways of cardiac regeneration
Jewhurst K, McLaughlin KA. Dev Growth Differ., 2019 Apr;61(3):212-227. doi: 10.1111/dgd.12602

53. Synchronization of Bioelectric Oscillations in Networks of Nonexcitable Cells: From Single-Cell to Multicellular States
Cervera, J., Manzanares, J. A., Mafe, S., and Levin, M.
Journal of Physical Chemistry B, 123: 3924-3934 [cover]

52. The Cognitive Lens: a primer on conceptual tools for analysing information processing in developmental and regenerative morphogenesis
Manicka, S., and Levin, M.
Phil. Trans. R. Soc. B, 374: 20180369

51. Neural control of body-plan axis in regenerating planaria
Pietak, A., Bischof, J., LaPalme, J., Morokuma, J., and Levin, M.
PLOS Computational Biology, doi: 10.1371/journal.pcbi.1006904

50. A Call for a Better Understanding of Causation in Cell Biology
Bizzari, M., Brash, D., Briscoe, J., Grieneisen, V., Stern, C. D., and Levin, M.
Nature Reviews Molecular Cell Biology, DOI: 10.1038/s41580-019-0127-1

49. Toward modeling regeneration via adaptable echo state networks
Hammelman, J., Siegelmann, H., Manicka, S., and Levin, M., in A. Adamatzky, S. Akl, and G. Sirakoulis (Eds.), From parallel to emergent computing, Chapter 6, pages 117-133, CRC Press

48. Effects of ivermectin exposure on regeneration of D. dorotocephala planaria: exploiting human-approved ion channel drugs as morphoceuticals
Ferenc, N. N., and Levin, M.
Macromolecular Bioscience, 19(3): 1800237 [cover]


47. EDEn – Electroceutical Design Environment: An Ion Channel Database with Small Molecule Modulators and Tissue Expression Information
Churchill, C. D. M., Winter, P., Tuszynski, J. A., and Levin, M.
iScience, 11: 42-56

46. Membrane potential depolarization alters calcium flux and phosphate signaling during osteogenic differentiation of human mesenchymal stem cells
Sundelacruz, S., Levin, M., and Kaplan, D.
Bioelectricity [in press]

45. The bacterial metabolite indole inhibits regeneration of the planarian flatwork Dugesia japonica
Lee, F. J., Williams, K. B., Levin, M., and Wolfe, B. E.
iScience, 10: 135-148

44. Brief Local Application of Progesterone via a Wearable Bioreactor Induces Long-Term Regenerative Response in Adult Xenopus Hindlimb
Herrera-Rincon, C., Golding, A. S., Moran, Harrison, C., Martyniuk, C. J., Guay, J. A., Zaltsman, J., Carabello, H., Kaplan, D. L., and Levin, M.
Cell Reports, 25: 1593-1609

43. Entropic effects in cell lineage tree packings
Jasmin Imran Alsous, Paul Villoutreix, Norbert Stoop, Stanislav Y. Shvartsman & Jörn Dunkel
Nature Physics, 14: 1016–1021 [cover]

42. Ivermectin promotes peripheral nerve regeneration during wound healing
Cairns, D. M., Giordano, J. E., Conte, S., Levin, M., and Kaplan, D. L.
ACS Omega, 3: 12392-12402

41. Activating PAX gene family paralogs to complement PAX5 leukemia driver mutations
Hart, M. R., Anderson, D. J., Porter, C. C., Neff, T., Levin, M., Horwitz, M. S.
PLoS Genetics, 4(9): e1007642

40. Cross-limb Communication During Xenopus Hind-limb Regenerative Response: Non-Local Bioelectric Injury Signals
Busse, S. M., McMillen, P. T., and Levin, M.
Development,145(19). pii: dev164210. doi: 10.1242/dev.164210

39. Inform: Efficient Information-Theoretic Analysis of Collective Behaviors
Moore, D. G., Valentini, G., Walker, S. I., and Michael Levin
Frontiers in Robotics and AI, 5(60) 1-14

38. Bioelectrical coupling in multicellular domains regulated by gap junctions: a conceptual approach
Cervera, J., Pietak, A., Levin, M., and Mafe, S.
Bioelectrochemistry 2018;123: 45-61 [cover]

37. Planarian Regeneration as a Model of Anatomical Homeostasis: Recent Progress in Biophysical and Computational Approaches
Michael Levin, Alexis M. Pietak, Johanna Bischof
Seminars in Cell and Developmental Biology [in press]

36. Bioelectrical control of positional information in development and regeneration: a review of conceptual and computational advances
Alexis Pietak and Michael Levin
Progress in Biophysics and Molecular Biology 137: 52-68

35. The Body Electric 2.0: Recent Advances in Developmental Bioelectricity for Regenerative and Synthetic Bioengineering
Juanita Mathews and Michael Levin
Curr Opin Biotechnol. 52: 134-144

34. Are planaria individuals? What regenerative biology is telling us about the nature of multicellularity
Fields C, Levin M
Evolutionary Biology. 2018;45:237–247. doi: 10.1007/s11692-018-9448-9

33. Embodying Markov blankets: Comment on “Answering Schrödinger’s question: A free-energy formulation” by Maxwell James Désormeau Ramstead et al.
Pezzulo G, Levin M
Phys Life Rev. 2018 Mar;24:32-36. doi: 10.1016/j.plrev.2017.11.020

32. Multiscale memory and bioelectric error correction in the cytoplasm-cytoskeleton-membrane system
Fields C, Levin M
Wiley Interdiscip Rev Syst Biol Med.2018 Mar;10(2). doi: 10.1002/wsbm.1410 [cover]

31. HCN2 Rescues brain defects by enforcing endogenous voltage pre-patterns
Pai VP, Pietak A, Willocq V, Ye B, Shi NQ, Levin M
Nat Commun. 2018 Mar 8;9(1):998. doi: 10.1038/s41467-018-03334-5

30. Inverse Drug Screening of Bioelectric Signaling and Neurotransmitter Roles: Illustrated Using a Xenopus Tail Regeneration Assay
Sullivan KG, Levin M
Cold Spring Harb Protoc. 2018 Mar 1;2018(3):pdb.prot099937. doi: 10.1101/pdb.prot099937

29. Booting up the organism during development: Pre-behavioral functions of the vertebrate brain in guiding body morphogenesis
Herrera-Rincon C, Levin M
Commun Integr Biol.
2018 Feb 15;11(1):e1433440. doi: 10.1080/19420889.2018.1433440 [cover]

28. The bioelectric code: An ancient computational medium for dynamic control of growth and form
Levin M, Martyniuk CJ
Biosystems. 2018 Feb;164:76-93. doi: 10.1016/j.biosystems.2017.08.009

27. Niclosamide rescues microcephaly in a humanized in vivo model of Zika infection using human induced neural stem cells
Cairns DM, Boorgu DSSK, Levin M, Kaplan DL
Biol Open. 2018 Jan 29;7(1). pii: bio031807. doi: 10.1242/bio.031807

26. Bioelectric signaling in regeneration: Mechanisms of ionic controls of growth and form
McLaughlin KA, Levin M
Dev Biol. 2018 Jan 15;433(2):177-189. doi: 10.1016/j.ydbio.2017.08.032


25. Identification of regenerative roadblocks via repeat deployment of limb regeneration in axolotls
Bryant DM, Sousounis K, Payzin-Dogru D, Bryant S, Sandoval AGW, Martinez Fernandez J, Mariano R, Oshiro R, Wong AY, Leigh ND, Johnson K, Whited JL
npj Regen Med. 2017 Nov 6;2:30. doi: 10.1038/s41536-017-0034-z

24. HCN4 Ion Channel Function is Required for Early Events that Regulate Anatomical Left-Right Patterning in a Nodal- and Lefty-Independent Manner
Pai VP, Willocq V, Pitcairn EJ, Lemire JM, Paré JF, Shi NQ, McLaughlin KA, Levin M
Biol Open. 2017 Oct 15;6(10):1445-1457. doi: 10.1242/bio.025957

23. Bioelectric gene and reaction networks: computational modelling of genetic, biochemical and bioelectrical dynamics in pattern regulation
Pietak A, Levin M
J R Soc Interface. 2017 Sep;14(134). pii: 20170425. doi: 10.1098/rsif.2017.0425 [cover]

22. The brain is required for normal muscle and nerve patterning during early Xenopus development
Herrera-Rincon C, Pai VP, Moran KM, Lemire JM, Levin M
Nat Commun. 2017 Sep 25;8(1):587. doi: 10.1038/s41467-017-00597-2

21. Collective Growth in a Small Cell Network
Imran Alsous J, Villoutreix P, Berezhkovskii AM, Shvartsman SY
Curr Biol. 2017 Sep 11;27(17):2670-2676.e4. doi: 10.1016/j.cub.2017.07.038

20. The Zahn Drawings: New Illustrations of Xenopus Embryo and Tadpole Stages for Studies of Craniofacial Development
Zahn N, Levin M, Adams DS
Development. 2017 Aug 1;144(15):2708-2713. doi: 10.1242/dev.151308 [cover]

19. Endogenous Bioelectric Signaling Networks: Exploiting Voltage Gradients for Control of Growth and Form
Levin M, Pezzulo G, Finkelstein JM
Annu Rev Biomed Eng. 2017 Jun 21;19:353-387. doi: 10.1146/annurev-bioeng-071114-040647

18. Planarian regeneration in space: persistent anatomical, behavioral, and bacteriological changes induced by space travel
Morokuma J, Durant F, Williams KB, Finkelstein JM, Blackiston DJ, Clements T, Reed DW, Roberts M, Jain M, Kimel K, Trauger SA, Wolfe BE, Levin M
Regeneration (Oxf). 2017 Jun 13;4(2):85-102. doi: 10.1002/reg2.79 [cover]

17. Bioelectric regulation of innate immune system function in regenerating and intact Xenopus laevis
Paré JF, Martyniuk CJ, Levin M
npj Regen Med. 2017 May 26;2:15. doi: 10.1038/s41536-017-0019-y

16. Long-term, stochastic editing of regenerative anatomy via targeting endogenous bioelectric gradients
Durant F, Morokuma J, Fields C, Williams K, Adams DS, Levin M
Biophys J. 2017 May 23;112(10):2231-2243. doi: 10.1016/j.bpj.2017.04.011 [cover]

15. Coordinating heart morphogenesis: a novel role for Hyperpolarization-activated cyclic nucleotide-gated (HCN) channels during cardiogenesis in Xenopus laevis
Pitcairn E, Harris H, Epiney J, Pai VP, Lemire JM, Ye B, Shi NQ, Levin M, McLaughlin KA.
Commun Integr Biol. 2017 May 10;10(3):e1309488. doi: 10.1080/19420889.2017.1309488. [cover]

14. Ion channel and neurotransmitter modulators as electroceutical approaches to the control of cancer
Tuszynski J, Tilli TM, Levin M
Curr Pharm Des. 2017;23(32):4827-4841. doi: 10.2174/1381612823666170530105837

13. Repeated removal of developing limb buds permanently reduces appendage size in
the highly-regenerative axolotl

Bryant DM, Sousounis K, Farkas JE, Bryant S, Thao N, Guzikowski AR, Monaghan JR, Levin M, Whited JL
Dev Biol. 2017 Apr 1;424(1):1-9. doi: 10.1016/j.ydbio.2017.02.013 [cover]

12. Serotonergic stimulation induces nerve growth and promotes visual learning via posterior eye grafts in a vertebrate model of induced sensory plasticity
Blackiston DJ, Vien K, Levin M.
npj Regen. Med. 2017 Mar 30; 8. doi:10.1038/s41536-017-0012-5

11. Reversals of bodies, brains, and behavior: quantitative analysis of laterality and its disturbance in model species,
Blackiston DJ and Levin M
in L. J. Rogers and G. Vallortigara (Eds.), Lateralized Brain Functions: Methods in Human and Non-human Species, “Neuromethods”, W. Walz (Ed.), 122: 667-694

10. Modeling regenerative processes with Membrane Computing
Garcia-Quismondo M, Levin M, Lobo, D
Information Sciences. 2017 381: 229-249. doi:10.1016/j.ins.2016.11.017

9. Discovering novel phenotypes with automatically inferred dynamic models: a partial melanocyte conversion in Xenopus
Lobo D, Lobikin M, Levin M
Sci Rep.2017 Jan 27;7:41339. doi: 10.1038/srep41339


8. Introduction to provocative questions in left-right asymmetry
Levin M, Klar AJ, Ramsdell AF
Philos Trans R Soc Lond B Biol Sci. 2016 Dec 19;371(1710). pii: 20150399 [cover]

7. From cytoskeletal dynamics to organ asymmetry: a nonlinear, regulative pathway underlies left-right patterning
McDowell G, Rajadurai S, Levin M
Philos Trans R Soc Lond B Biol Sci. 2016 Dec 19;371(1710). pii: 20150409

6. Top-down models in biology: explanation and control of complex living systems
above the molecular level

Pezzulo G, Levin M
J R Soc Interface. 2016 Nov;13(124). pii: 20160555

5. Vertically- and horizontally-transmitted memories – the fading boundaries between regeneration and inheritance in planaria
Neuhof M, Levin M, Rechavi O
Biol Open. 2016 Sep 15;5(9):1177-88. doi: 10.1242/bio.020149 [cover]

4. Physiological inputs regulate species-specific anatomy during embryogenesis and

Sullivan KG, Emmons-Bell M, Levin M
Commun Integr Biol. 2016 Jul 15;9(4):e1192733. doi: 10.1080/19420889.2016.1192733

3. Exploring Instructive Physiological Signaling with the Bioelectric Tissue Simulation Engine
Pietak A, Levin M
Front Bioeng Biotechnol. 2016 Jul 6;4:55. doi: 10.3389/fbioe.2016.00055

2. A computational model of planarian regeneration
De A, Chakravarthy VS, Levin M
International Journal of Parallel, Emergent and Distributed Systems. 2016 May 24:1-7. doi:10.1080/17445760.2016.1185521

1. Physiological controls of large-scale patterning in planarian regeneration: a molecular and computational perspective on growth and form
Durant F, Lobo D, Hammelman J, Levin M
Regeneration (Oxf). 2016 Apr 28;3(2):78-102. doi: 10.1002/reg2.54 [cover]