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• Published: 15 March 2024

Fine tuning of CpG spatial distribution with DNA origami for improved cancer vaccination

• Yang C. Zeng   ORCID: orcid.org/0000-0003-0566-4976 1 , 2 , 3 ,
• Olivia J. Young 1 , 2 , 3 , 4 ,
• Christopher M. Wintersinger   ORCID: orcid.org/0000-0003-4633-9651 1 , 3 ,
• Frances M. Anastassacos 2 , 3 ,
• James I. MacDonald 2 ,
• Giorgia Isinelli   ORCID: orcid.org/0000-0002-1798-1576 2 , 5 ,
• Maxence O. Dellacherie 6 ,
• Miguel Sobral 6 ,
• Haiqing Bai 2 ,
• Amanda R. Graveline 2 ,
• Andyna Vernet 2 ,
• Melinda Sanchez 2 ,
• Kathleen Mulligan 1 ,
• Youngjin Choi 7 ,
• Thomas C. Ferrante 2 ,
• Derin B. Keskin 8 ,
• Geoffrey G. Fell 9 ,
• Donna Neuberg   ORCID: orcid.org/0000-0003-2566-3145 9 ,
• Catherine J. Wu   ORCID: orcid.org/0000-0002-3348-5054 8 ,
• David J. Mooney   ORCID: orcid.org/0000-0001-6299-1194 2 , 6 ,
• Ick Chan Kwon   ORCID: orcid.org/0000-0003-1272-7074 1 , 7 , 10 ,
• Ju Hee Ryu   ORCID: orcid.org/0000-0003-3422-3272 1 , 7 &
• William M. Shih   ORCID: orcid.org/0000-0002-1395-9267 1 , 2 , 3  

Nature Nanotechnology ( 2024 ) Cite this article

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• Drug delivery
• Nanostructures

Multivalent presentation of ligands often enhances receptor activation and downstream signalling. DNA origami offers a precise nanoscale spacing of ligands, a potentially useful feature for therapeutic nanoparticles. Here we use a square-block DNA origami platform to explore the importance of the spacing of CpG oligonucleotides. CpG engages Toll-like receptors and therefore acts to activate dendritic cells. Through in vitro cell culture studies and in vivo tumour treatment models, we demonstrate that square blocks induce Th1 immune polarization when CpG is spaced at 3.5 nm. We observe that this DNA origami vaccine enhances DC activation, antigen cross-presentation, CD8 T-cell activation, Th1-polarized CD4 activation and natural-killer-cell activation. The vaccine also effectively synergizes with anti-PD-L1 for improved cancer immunotherapy in melanoma and lymphoma models and induces long-term T-cell memory. Our results suggest that DNA origami may serve as a platform for controlling adjuvant spacing and co-delivering antigens in vaccines.

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Data availability

Data supporting the findings of this study are available in the Article and its Supplementary Information . The RNAseq data for the stimulated BMDCs generated and analysed in this Article have been deposited in NCBI’s Gene Expression Omnibus under accession no. GSE251850 . Source data are provided with this paper.

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Acknowledgements

We thank Q. Yan, Z. Zhao, T. Zhang, P. Lill, P. Prabhala, L. Chou, J. Han, D. Minev, B. Everhart, J. Deng, D. Zhang, K. Adu-Berchie, H. Dembele, A. Rajwar and K. Simpson for aiding in labour support, experimental design, exploring experiments and manuscript proofreading. We also thank M. Perez, M. Carr and E. Zigon for their assistance in lab management and facility usage. We thank M. Bastings and A. Li for exploration—before the current project initiated—of CpG-functionalized DNA origami barrels for immune stimulation. This work was funded by the Barr Award granted by the Claudia Adams Barr Program (Y.C.Z.) in the Dana-Farber Cancer Institute and by Wyss validation funding (Y.C.Z.) at the Wyss Institute for Biologically Inspired Engineering at Harvard. This study was supported by the Korean Fund for Regenerative Medicine (J.H.R.; 21A0504L1) funded by the Korean government (the Ministry of Science and ICT and the Korean Ministry of Health & Welfare) and the Intramural Research Program of KIST (J.H.R.; no. 2E30840). This project was also supported by an NIH U54 grant (W.M.S.; CA244726-01).

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Authors and affiliations.

Department of Cancer Biology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA

Yang C. Zeng, Olivia J. Young, Christopher M. Wintersinger, Kathleen Mulligan, Ick Chan Kwon, Ju Hee Ryu & William M. Shih

Wyss Institute for Biologically Inspired Engineering at Harvard University, Boston, MA, USA

Yang C. Zeng, Olivia J. Young, Frances M. Anastassacos, James I. MacDonald, Giorgia Isinelli, Haiqing Bai, Amanda R. Graveline, Andyna Vernet, Melinda Sanchez, Thomas C. Ferrante, David J. Mooney & William M. Shih

Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USA

Yang C. Zeng, Olivia J. Young, Christopher M. Wintersinger, Frances M. Anastassacos & William M. Shih

Harvard-Massachusetts Institute of Technology (MIT) Division of Health Sciences and Technology, Massachusetts Institute of Technology, Cambridge, MA, USA

Olivia J. Young

Department of Drug and Health Sciences, University of Catania, Catania, Italy

Giorgia Isinelli

Harvard John A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA, USA

Maxence O. Dellacherie, Miguel Sobral & David J. Mooney

Center for Theragnosis, Biomedical Research Institute, Korea Institute of Science and Technology (KIST), Seoul, Republic of Korea

Youngjin Choi, Ick Chan Kwon & Ju Hee Ryu

Department of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA, USA

Derin B. Keskin & Catherine J. Wu

Department of Data Science, Dana-Farber Cancer Institute, Boston, MA, USA

Geoffrey G. Fell & Donna Neuberg

KU-KIST Graduate School of Converging Science and Technology, Korea University, Seoul, Republic of Korea

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Contributions

Y.C.Z. developed and planned the experiments, carried out the vaccine fabrication and validation, and wrote the manuscript. J.H.R. and W.M.S. provided the experimental and theoretical guidance and edited the manuscript. O.J.Y. assisted Y.C.Z. in performing the experiments, analysing the data and manuscript editing. C.M.W., F.M.A., J.I.M. and G.I. assisted with the DNA origami design, modelling and fabrication. H.B. performed the RNAseq analysis. M.O.D., M. Sobral, M. Sanchez, A.R.G. and A.V. helped with the animal study design, modelling and sampling. T.C.F. assisted with the confocal experiment. Y.C. assisted with the 3D modelling and manuscript editing. G.G.F. and D.N. guided the statistical analysis. C.J.W. and D.B.K. guided the experiment design and offered manuscript editing. D.J.M. and I.C.K. provided project support and manuscript editing.

Corresponding authors

Correspondence to Ju Hee Ryu or William M. Shih .

Ethics declarations

Competing interests.

W.M.S., J.H.R. and Y.C.Z. are inventors on US patent application PCT/US2020/036281 held by Dana-Farber Cancer Institute, Korea Institute of Science and Technology and Wyss Institute (filed on 5 June 2020) partially based on this work. All other authors declare no competing interests.

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Nature Nanotechnology thanks Mark Bathe, Diana Morzy and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

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Supplementary Figs. 1–34, Tables 1–6, Discussion and Methods.

Reporting Summary

Supplementary Video 1 This video demonstrates the effective uptake of DNA origami nanoparticles coated with K10-PEG5k by DCs within a time frame of 2 h and reveals the presence of DNA origami nanoparticles (pink) conjugated with OVA antigen (green) within the DCs, along with late endosomes (cyan).

Supplementary Data 1

Statistical source data.

Supplementary Data 2

Supplementary data 3, supplementary data 4, supplementary data 5, supplementary data 6, supplementary data 7, supplementary data 8, supplementary data 9, supplementary data 10, supplementary data 11, supplementary data 12, supplementary data 13, supplementary data 14, supplementary data 15, supplementary data 16, supplementary data 17, supplementary data 18, supplementary data 19, supplementary data 20, source data, source data fig. 1, source data fig. 2, source data fig. 3, source data fig. 4, source data fig. 5, source data fig. 6, rights and permissions.

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Zeng, Y.C., Young, O.J., Wintersinger, C.M. et al. Fine tuning of CpG spatial distribution with DNA origami for improved cancer vaccination. Nat. Nanotechnol. (2024). https://doi.org/10.1038/s41565-024-01615-3

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Published : 15 March 2024

DOI : https://doi.org/10.1038/s41565-024-01615-3

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Watch the crazy AI short films and videos created by artists with early access to OpenAI's Sora tool

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And they are being ravaged by a sexually transmitted disease that turns them into zombies.

PUMPS IN THE HEAD

Inside trees are sugary, nutrient-heavy saps that flow through tissue called phloem. Most insects love the sap. But not cicadas — they go for tissue called xylem, which carries mostly water and a bit of nutrients.

And it's not easy to get into the xylem, which doesn't just flow out when a bug taps into it because it's under negative pressure. The cicada can get the fluid because its outsized head has a pump, said University of Alabama Huntsville entomologist Carrie Deans.

They use their proboscis like a tiny straw — about the width of a hair — with the pump sucking out the liquid, said Georgia Tech biophysics professor Saad Bhamla. They spend nearly their entire lives drinking, year after year.

“It's a hard way to make a living,” Deans said.

GOING WITH THE FLOW

All that watery fluid has to come out the other end. And boy does it.

Bhamla in March published a study of the urination flow rates of animals across the world. Cicadas were clearly king, peeing two to three times stronger and faster than elephants and humans. He couldn't look at the periodical cicadas that mostly feed and pee underground, but he used video to record and measure the flow rate of their Amazon cousins, which topped out around 10 feet per second (3 meters per second).

They have a muscle that pushes the waste through a tiny hole like a jet, Bhamla said. He said he learned this when in the Amazon he happened on a tree the locals called a “weeping tree” because liquid was flowing down, like the plant was crying. It was cicada pee.

“You walk around in a forest where they're actively chorusing on a hot sunny day. It feels like it's raining,” said University of Connecticut entomologist John Cooley. That's their honeydew or waste product coming out the back end ... It's called cicada rain."

GOOD FOR CATERPILLARS

In the years and areas where cicadas come out, caterpillars enjoy a cicada reprieve.

University of Maryland entomologist Dan Gruner studied caterpillars after the 2021 cicada emergence in the mid-Atlantic. He found that the bugs that turn into moths survived the spring in bigger numbers because the birds that usually eat them were too busy getting cicadas.

Periodical cicadas are “lazy, fat and slow,” Gruner said. “They're extraordinarily easy to capture for us and for their predators.”

ZOMBIE CICADAS

There's a deadly sexually transmitted disease, a fungus, that turns cicadas into zombies and causes their private parts to fall off, Cooley said.

It's a real problem that “is even stranger than science fiction,” Cooley said. “This is a sexually transmitted zombie disease.”

Cooley has seen areas in the Midwest where up to 10% of the individuals were infected.

The fungus is also the type that has hallucinatory effects on birds that would eat them, Cooley said.

This white fungus takes over the male, their gonads are torn from their body and chalky spores are spread around to nearby other cicadas, he said. The insects are sterilized, not killed. This way the fungus uses the cicadas to spread to others.

“They're completely at the mercy of the fungus,” Cooley said. “They're walking dead.”

Read more of AP’s climate coverage at http://www.apnews.com/climate-and-environment

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The Associated Press’ climate and environmental coverage receives financial support from multiple private foundations. AP is solely responsible for all content. Find AP’s standards for working with philanthropies, a list of supporters and funded coverage areas at AP.org.

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🏀 Men's Tournament

🎟️ Final Four set

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NCAA | March 31, 2024

Minnesota state wins the 2024 ncaa division ii men's basketball championship.

Minnesota State is the 2024 NCAA Division II men's basketball champion after beating Nova Southeastern 88-85 off a game-winning three pointer with less than a second on the clock.

This victory came one day after the Minnesota State women won their respective title .

WHAT A SHOT WITH 0.6 LEFT 😱😱 WILLINGHAM FROM THE CORNER @MinnStMBBall !!!! pic.twitter.com/rvW3RdSGT0 — CBS Sports College Basketball 🏀 (@CBSSportsCBB) March 30, 2024

2024 NCAA DII men's basketball championship bracket

The DII men's basketball tournament continues through the championship game on Saturday, March 30:

Click or tap here for the printable bracket ➡️

2024 NCAA DII men's basketball championship schedule

*All times in Eastern

National Championship: Saturday, March 30

• (1) Minnesota State 88,  (2) Nova Southeastern 85

March 15 | Regional quarterfinals

• (1) Gannon 97, (8) Lincoln (PA) 63  | WATCH FULL REPLAY
• (2) California (PA) 96, (7) West Virginia State 80  | WATCH FULL REPLAY
• (4) West Liberty 100, (5) Millersville 78  | WATCH FULL REPLAY
• (3) Charleston (WV) 93,  vs. (6) Concord 55  | WATCH FULL REPLAY
• ( 6) Chico State 78, (3) Mont. St. Billings 64  | WATCH FULL REPLAY
• (2) CSUSB 52,  (7) Alaska Anchorage 49  | WATCH FULL REPLAY
• (8) Azusa Pacific 60, (1) Cal State LA 59  | WATCH FULL REPLAY
• (5) Central Washington 110, (4) Cal St. Dom. Hills 90  | WATCH FULL REPLAY

March 16 | Regional semifinals

• (1) Gannon 103,  (4) West Liberty 88  | WATCH FULL REPLAY
• (3) Charleston (WV) 68, (2) California (PA) 67  | WATCH FULL REPLAY
• (2) CSUSB 75,  (6) Chico State 73  | WATCH FULL REPLAY
• (8) Azusa Pacific 82, (5) Central Washington 74  | WATCH FULL REPLAY

March 16 | Regional quarterfinals

• (3) Minnesota Duluth 59,  (6) Fort Hays State 58  | WATCH FULL REPLAY
• (2) Northwest Missouri State 73, (7) Southwest Minn. State 43  | WATCH FULL REPLAY
• (1) Minnesota State 75,  (8) Arkansas Tech 68  | WATCH FULL REPLAY
• ( 4) MSU Moorhead 73 , (5) Pittsburgh State 55  | WATCH FULL REPLAY
• (3) Southern New Hampshire 75 , (6) Bloomfield 70  | WATCH FULL REPLAY
• (7) Post 80, (2) St. Thomas Aquinas 72  | WATCH FULL REPLAY
• (1) Saint Michael's 68,  (8) Southern Connecticut State 62  | WATCH FULL REPLAY
• (4) Daemen 74,  (5) Jefferson 66  | WATCH FULL REPLAY
• (6) Lake Superior State 74,   (3) Walsh 72  | WATCH FULL REPLAY
• (7) Upper Iowa 82, (2) Kentucky Wesleyan 72  | WATCH FULL REPLAY
• (1) Uindy 71,  (8) William Jewell 65  | WATCH FULL REPLAY
• (5) Ferris State 81,  (4) Northern Michigan 65  | WATCH FULL REPLAY
• (3) Florida Southern 80,  (6) Clark Atlanta 72  | WATCH FULL REPLAY
• (2) West Georgia 75,  (7) Lee 61  | WATCH FULL REPLAY
• (1) Nova Southeastern 115,  (8) Benedict 95  | WATCH FULL REPLAY
• (5) Embry-Riddle (FL) 104,  (4) Alabama Huntsville 78   | WATCH FULL REPLAY
• (6) Lander 85 , (3) Lincoln Memorial 76  | WATCH FULL REPLAY
• (7) Emmanuel (GA) 70 , (2) USC Aiken 69   | WATCH FULL REPLAY
• (1) North Georgia 89,  (8) Wingate 80  | WATCH FULL REPLAY
• (5) UNC Pembroke 98, (4) Catawba 94  OT  | WATCH FULL REPLAY

South Central

• (3) Colorado Mesa 95,   (6) Eastern New Mexico 77  | WATCH FULL REPLAY
• (2) Fort Lewis 86,  (7) Lubbock Christian. 72  | WATCH FULL REPLAY
• (1) West Texas A&M 81,  (8) Angelo State 66  | WATCH FULL REPLAY
• (4) DBU 86, (5) Colorado School of Mines 73  | WATCH FULL REPLAY

March 17 | Regional semifinals

• (3) Northwest Missouri State 71,  (2) Minnesota Duluth 62  | WATCH FULL REPLAY
• (1) Minnesota State 78,  (4) MSU Morehead 55  | WATCH FULL REPLAY
• (3) Southern New Hampshire 69,  (7) Post 64  | WATCH FULL REPLAY
• (1) St. Michael's 86,  (4) Daemen 62  | WATCH FULL REPLAY
• (6) Lake Superior State 88,  (7) Upper Iowa 80  | WATCH FULL REPLAY  
• (5) Ferris State 94,  (1) UIndy 87 OT  | WATCH FULL REPLAY
• (3) Florida Southern 93,  (2) West Georgia 87 OT  | WATCH FULL REPLAY
• (1) Nova Southeastern 81, (5) Embry-Riddle 73  | WATCH FULL REPLAY  
• (6) Lander 86,  (7) Emmanuel (GA) 78 OT  | WATCH FULL REPLAY
• (1) UNG 86,  (4) Catawba 70  | WATCH FULL REPLAY  
• (3) Colorado Mesa 85, (2) Fort Lewis 80  | WATCH FULL REPLAY
• (1) West Texas A&M 60,  (4) DBU 54  | WATCH FULL REPLAY  

March 18 | Regional finals

• (2) CSUSB 74, (8) Azusa Pacific 67   | WATCH FULL REPLAY

March 19 | Regional finals

• (3) Southern N. H. 73,   (1) Saint Michael's 61
• (1) Nova Southeastern 98,  (3) Florida Southern 66  
• (1) North Georgia 70,   Lander 67
• (5) Ferris St. 86, (6) Lake Superior 81
• (1) Minnesota St. 43, Northwest Missouri St. 42
• (1) Gannon 67,  (3) Charleston (WV) 65
• (1) West Texas A&M 88, (3) Colorado. Mesa 76

March 26 | Quarterfinals 

• (6) CSUSB 99, (3) Gannon 65 | WATCH FULL REPLAY
• (2) Nova Southeastern 68, (7) Southern N.H. 60 | WATCH FULL REPLAY
• (1) Minnesota St. 98, (8) Ferris St 70  | WATCH FULL REPLAY
• (4) West Tex. A&M 90 ,  (5) North Georgia 76  | WATCH FULL REPLAY

March 28 |Semifinals

• (2) Nova Southeastern 91,  (6) CSUSB 77   | WATCH FULL RECAP
• (1) Minnesota St. 79,   (4) West Tex. A&M 72    | WATCH FULL RECAP

How to watch

NCAA Championships Pass will stream 120 DII men’s and women’s basketball tournament games (all games from first round through quarterfinals) live on NCAA.com. Games will be available on NCAA.com , school sites that stream through Hudl and opt to co-distribute the live streams, and the NCAA Championships Pass app available for Roku, Apple TV, Amazon Fire TV, and Google TV.

Prices for viewing (first round through quarterfinals)

• $9.95 per game
• $29.95 per championship
• $49.95 for all games

Semifinals and finals viewing

• Semifinals: Thursday, March 28 on CBS Sports Network (2p ET, 4:30p)
• Championship: Saturday, March 30 on CBS (3p ET)

🎟️ Get NCAA Championships Pass

DII NCAA men's basketball championship history

The Division II men's basketball championship consists of a 64-team field with eight qualifiers from each region competing at a single regional site. Twenty-three teams earn automatic qualifications and the remaining 41 receive at-large bids to the tournament. Once the eight regionals conclude, respective teams will advance to the Men's Elite Eight at the Ford Center in Evansville, Indiana.

The DII men's basketball national championship dates back to 1957, skipping 2020 due to COVID-19, with the first-ever championship trophy going to Wheaton (Ill.). Kentucky Wesleyan is the winningest team, with eight national championships. Evansville follows with five titles.

Below is a list of all DII men's basketball champs since 1957:

**Student-athletes declared ineligible

What defines UConn, Purdue, Alabama and NC State's path to the 2024 Men's Final Four

Purdue heads to the Final Four, starting a celebration 44 years in the making

2024 March Madness: Men's NCAA tournament schedule, dates

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